Central Cholinergic Synaptic Transmission

332 Pages·1989·6.18 MB·English

by  M.-Marsel Mesulam (auth.)

Central Cholinergic
Synaptic Transmission
Edited by Michael Frotscher
Ulrich Misgeld
1989
Birkhiuser Verlag
Basel • Boston . Berlin
Editors:
Prof. Dr. Michael Frotscher Priv.-Doz. Dr. Ulrich Misgeld
Anatomisches Institut Max-Planck-Institut fiir
J. W. Goethe-Universitit Psychiatrie
Theodor-Stern-Kai 7 Am Klopferspitz 18A
6000 Frankfurt a.M. 70 8033 Planegg-Martinsried
Federal Republic of Germany Federal Republic of Germany
Library of Congress Cataloging In PubUeation Data
Central cholinergic synaptic transmission/edited by Michael
Frotscher, Ulrich Misgeld.
p. cm.-(Experientia. Supplementum: vol. 57
Includes index.
ISBN-13: 978-3-0348-9922-2 e-ISBN-13: 978-3-0348-9138-7
DOl: 10.1007/978-3-0348-9138-7
I. Neural transmission. 2. Acetylcholine-Receptors.
3. Cholinergic mechanisms. 4. Central nervous system.
I. Frotscher, Michael, 1947- . II. Misgeld, Ulrich, 1943-
III. Series: Experientia. Supplementum: v. 57.
[DNLM: I. Neural Transmission. 2. Neuroregulators. 3. Receptors,
Cholinergic. 4. Synapses-physiology. WI EX23 v. 57/WL 102.8
C3975]
OP364.7.C46 1989
599.0188-<:d19
DNLM/DLC
CIP-Tltelanfnahme der Deutseben BlbUotbek
Central dIolinergic synaptle tnmsmIssIon/ed. by Michael
Frotscher; Ulrich Misgeld.-Basel; Boston; Berlin:
Birkhauser, 1989
(Experientia: Supplementum; Vol. 57)
NE: Frotscher, Michael [Hrsg.]; Experientia/Supplementum
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© 1989 Birkhiuser Verlag
Softcover reprint of the hardcover 1st edition 1989
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v
Contents
Preface ................................................... ix
Cholinergic neurons, pathways and synapses
M.-M. Mesulam
Behavioral neuroanatomy of cholinergic innervation in the
primate cerebral cortex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. I
L. Zaborszky
Afferent connections of the forebrain cholinergic projection
neurons, with special reference to monoaminergic and
peptidergic fibers ............. ~ . . . . . . . . . . . . . . . . . . . . . . . . . .. 12
M. Frotscher
Central cholinergic synapses: The septohippocampal system
as a model .............................................. 33
L. Nitecka and M. Frotscher
Cholinergic-GABAergic synaptic interconnections in the rat
amygdaloid complex: An electron microscopic double
immunostaining study . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 42
G. Raivich and G. W. Kreutzberg
Topography of f3NGF receptor-positive and AChE-reactive
neurons in the central nervous system ....................... 50
E. Borroni, E. Derrington and V. P. Whittaker
Chol-l: A cholinergic-specific ganglioside of possible
significance in central nervous system neurochemistry and
neuropathology .......................................... 59
Acetylcholine-induced postsynaptic potentials and excitatory changes
P. Dutar and R. A. Nicoll
Pharmacological characterization of muscarinic responses in
rat hippocampal pyramidal cells ............................ 68
N. Agopyan, K. Krnjevic and J. Leblond
Mediation of acetylcholine's excitatory actions in central
neurons ................................................. 77
vi
M. Segal, V. Greenberger and H. Markram
Presynaptic cholinergic action in the hippocampus .............. 88
M. Toselli and H. D. Lux
Opposing effects of acetylcholine on the two classes of
voltage-dependent calcium channels in hippocampal
neurons ................................................. 97
U. Misgeld
Muscarinic slow EPSPs in neostriatal and hippocampal
neurons in vitro ......................................... 104
w. Milller and U. Misgeld
Carbachol and pirenzepine discriminate effects mediated by
two muscarinic receptor subtypes on hippocampal neurons
in vitro .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 114
R. W. Greene, H. L. Haas, U. Gerber and R. W. McCarley
Cholinergic activation of medial pontine reticular formation
neurons in vitro ......................................... 123
J. V. Halliwell
Cholinergic responses in human neocortical neurones .......... 138
Y. Yaari and M. S. Jensen
Cholinergic modulation of hippocampal epileptic activity in
vitro ................................................... 150
G. Buzsaki and F. H. Gage
The cholinergic nucleus basalis: A key structure in
neocortical arousal ...................................... 159
C. M. Milller
Cholinergic mechanisms in the telencephalon of cat and
chicken ................................................ 172
Cholinergic receptor types and their modulation
H. Betz, E. D. Gundelfinger, l. Hermans-Borgmeyer,
E. Sawruk, P. Schloj and B. Schmitt
Central nicotinic acetylcholine receptors in the chicken and
Drosophila CNS: Biochemical and molecular biology
approaches ............................................. 183
T. Akasu and T. Tokimasa
Modulation of the sensitivity of nicotinic receptors in
autonomic ganglia ....................................... 190
vii
H. Kilbinger, H. Schworer and K. D. Sufi
Muscarinic modulation of acetylcholine release: Receptor
subtypes and possible mechanisms ......................... 197
M. H. Weiler
Characterization of muscarinic receptors modulating
acetylcholine release in the rat neostriatum ................. 204
K. Zilles, H. Schroder, U. Schroder, E. Horvath, L. Werner,
P. G. M. Luiten, A. Maelicke and A. D. Strosberg
Distribution of cholinergic receptors in the rat and human
neocortex .............................................. 212
Acetylcholine and plasticity of the eNS
D. J. Jenden, R. W. Russel, R. A. Booth, B. J. Knusel,
S. D. Lauretz, K. M. Rice and M. Roch
Effects of chronic in vivo replacement of choline with a false
cholinergic precursor ..................................... 229
B. H. Giihwiler, D. A. Brown, A. Enz and T. Knopfel
Development of the septohippocampal projection in vitro ....... 236
C. Grothe, D. Otto, M. Frotscher and K. Unsicker
A role of basic fibroblast growth factor for rat septal
neurons ................................................ 251
F. H. Gage, M. H. Tuszynski, K. S. Chen, D. Armstrong and
G. Buzsaki
Survival, growth and function of damaged cholinergic
neurons ................................................ 259
D. J. Clarke and A. Bjorklund
Restoration of cholinergic circuitry in the hippocampus by
foetal grafts ............................................ 275
A. Represa and Y. Ben-Ari
Effects of colchicine treatment on the cholinergic
septohippocampal system ................................. 288
C. Walch, R. Schliebs and V. Bigl
Effect of early visual pattern deprivation on development
and laminar distribution of cholinergic markers in rat
visual cortex ............................................ 295
viii
Q. Gu and W. Singer
The role of muscarinic acetylcholine receptors in ocular
dominance plasticity ..................................... 305
P. Calabresi, A. Stefani, N. B. Mercuri and G. Bernardi
Acetylcholine-dopamine balance in striatum: Is it still a
target for antiparkinsonian therapy? ....................... 315
Preface
Our knowledge of cholinergic synaptic transmission in the peripheral
nervous system (PNS) has expanded enormously since the early 1930's,
at which time O. Loewi discovered chemical neurotransmission through
acetylcholine (ACh) and the pharmacological actions of ACh were
described by H. Dale and his colleagues. Description of ACh's actions
and receptors in various parts of the brain was followed by a detailed
analysis of ACh's synthesis, release mechanism, removal from the
synaptic cleft, modes of agonist-receptor interactions, properties of
regulated conductances and of the pre- and postsynaptic modulation of
cholinergic synapses. Our knowledge has been increasingly consolidat
ing, leading us to the recent clarification of the structure of the periph
eral nicotinic receptor-ion channel and its functional properties. It is
appropriate to maintain the claim that the fundamentals of our under
standing of synaptic transmission come from studies on cholinergic
synapses in the PNS.
Contrastingly, views held on the role of cholinergic synapses in the
mammalian central nervous system (CNS) are extremely controversial,
although it has been clear for some time that ACh is present in the
brain. Illustrating this, no unanimous view is held on the role of
nicotinic receptors in the CNS. There is one notable exception to this
confusion: Studies begun by J. C. Eccles and associates in the 1960's and
completed by D. R. Curtis and R. W. Ryall in the 1970's on the motor
axon collateral-Renshaw cell pathway in cats revealed the same princi
ples of cholinergic synaptic transmission in the spinal cord as those
revealed in studies on neuro-neuronal synapses in autonomic ganglia. In
both autonomic ganglia and brain, however, the functional role of
'slow' muscarinic transmission is unknown.
The main obstacle to a better understanding of central cholinergic
synaptic transmission is nothing less than the complexity of the brain
itself. However, fundamental information provided by studies on
peripheral cholinergic synaptic transmission strongly suggests that cen
tral cholinergic synaptic transmission is a key to understanding central
synaptic transmission in general. The significance of cholinergic synaptic
mechanisms is also weightened by the possibility that they may have a
pivotal role in CNS disorders such as Alzheimer's disease.
New techniques and new tools, particularly those developed in the
last decade, facilitated the discovery of many new facts concerning
cholinergic synaptic transmission in the CNS. Choline acetyl transferase
x
immunocytochemistry and various in vitro preparations of the mam
malian CNS, with the aid of refined electrophysiological techniques, are
just a few examples. Other techniques, single channel recording and
molecular biology approaches, are beginning to show their potential
usefulness. Given this state of methodological advancement, we consid
ered it worthwhile to collect current views held on central cholinergic
synaptic transmission.
This book is the manifestation of that collection of views. Most of the
articles were first presented at a meeting with the same title in Septem
ber, 1988 at Ringberg Castle in Bavaria. The book starts with a series of
morphological studies on the distribution of cholinergic neurons, the
course of cholinergic fibers and the ultrastructural features of choliner
gic synapses in the CNS. Following this, a series of electrophysiological
studies are presented centering around synaptic responses, involvement
of various receptor types and their coupling to second messengers. The
third group of articles introduces molecular biology techniques and
pharmacological approaches for the study of receptors. Finally, there is
a series of studies dealing with the influence of environmental cues on
growth and regrowth of cholinergic fibers and the involvement of
cholinergic systems in the plastiCity of the brain.
This book does not aim to resolve all matters of controversy on the
topic. On the contrary, the reader will find a number of controversial
and even contradicting statements in the different articles. The book
does, however, provide a comprehensive account of 'state of the art'
research on central cholinergic synaptic transmission, which we hope
will prove provoking and stimulating for future research.
The editors wish to thank the Stiftung Volkswagenwerk, the Univer
sity of Frankfurt, the Sonderforschungsbereich 45 and 220 of the
Deutsche Forschungsgemeinschaft, the Dr. Ernst-Rudolf SchloeBmann
Stiftung, the Max-Planck-Gesellschaft, CIBA-Geigy GmbH, Hoffmann
La Roche AG, E. Merck, Sandoz AG, and Boehringer Ingelheim KG
for making the meeting previous to the preparation of this book
possible, and Birkhauser Verlag for its publication. Special thanks to E.
Schroeder for her organizational and editorial assistance.
M. Frotscher and U. Misgeld
Behavioral neuroanatomy of cholinergic
innervation in the primate cerebral cortex
M.-Marsel Mesulam
Department of Neurology, Beth Israel Hospital, JJO Brookline Avenue, Boston, MA 02215, USA
Summary. This brief review summarizes the anatomy and behavioral affiliations of cortical
cholinergic innervation. A depletion of this innervation has been reported in a number of
human neurodegenerative conditions (including Alzheimer's disease) and may contribute to
the genesis of the associated behavioral disturbances.
Central cholinergic pathways have been implicated in the regulation
of extrapyramidal motor function, arousal, sleep, mood and especially
memory (Karczmar, 1975). In keeping with the diversity of these
behavioral affiliations, cholinergic pathways reach all levels of the
neuraxis. Although ubiquitous, these pathways also display a strict
topographical arrangement. Modern methods for axonal tracing and
immunohistochemistry have led to the accumulation of additional infor
mation on the anatomical organization of these pathways.
The cholinergic innervation of the striatal complex is predominantly
intrinsic and originates from cholinergic interneurons (Woolfe and
Butcher, 1981). In contrast, the cholinergic innervation of the cerebral
cortex, amygdaloid nuclei, olfactory bulb, thalamus and mesencephalic
tectum is almost exclusively extrinsic, at least in the adult primate. The
hippocampal formation receives its major cholinergic innervation from·
the medial septal nucleus (the cholinergic neurons of which are also
designated as ChI) and the vertical limb nucleus of the diagonal band
(Ch2); the olfactory bulb from the horizontal limb nucleus of the
diagonal band (Ch3); the cerebral cortex and amygdaloid nuclei from
the nucleus basalis (Ch4); the thalamus from the pedunculopontine
(Ch5) and laterodorsal tegmental nuclei (Ch6); the interpeduncular
nucleus from the medial habenula (Ch7) and the superior colliculus
from the parabigeminal nucleus (Ch8) (Mesulam et aI., 1983a, b;
Mufson et aI., 1986).
The cholinergic nature of the nucleus basalis (NB) neurons has been
demonstrated in a large number of animal species by showing the
presence of an AChE-rich and ChAT-positive staining pattern (Wainer
et aI., 1984). In both man and monkey, more than 90% of the magno
cellular NB neurons are also ChAT-positive (Mesulam et aI., 1983a;
Mesulam and Geula, 1988). These observations justify the designation