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Journal of Neuroscience, Vol 6, 1061-1079, Copyright © 1986 by Society for Neuroscience
Synaptic functions in rat sympathetic neurons in microcultures. I. Secretion of norepinephrine and acetylcholine
EJ Furshpan, SC Landis, SG Matsumoto and DD Potter
This is the first of a series of four papers that describes the use of a
sensitive "microculture" procedure for examining the neurotransmitter
profile of a neuron by assaying the transmitter(s) it releases. Sympathetic
principal neurons isolated from the superior cervical ganglia of neonatal
or adult rats were grown for 10 d to several months on small islands of
cardiac myocytes (island diameter, ca. 0.5 mm). To assay transmitter status
a neuron and a myocyte in the same microculture were impaled with
microelectrodes, the neuron was stimulated and the pharmacology of the
effect(s) on the group of electrically coupled myocytes, and on the neuron
itself, was investigated. Because the growing axonal processes were
confined to the island, the innervation of the myocytes became dense;
transmission from neuron to myocytes occurred reliably and was often
intense. Most experiments were done on islands containing only a single
neuron so that the observed effect(s) on the myocytes could be confidently
assigned to that neuron. After the physiological assay, the fine structure
or cytochemistry of the neuron was often examined. With single-neuron
microcultures the physiology and anatomy of the neuron, including the fine
structure of its synaptic endings and varicosities, could be correlated
unambiguously. During the course of this work, we have observed five
pharmacologically distinct effects exerted on the myocytes by either
neonate- or adult-derived neurons. Three of these effects, one exerted at
least in large part by adenosine and the others by agents still under study
(one appears to be 5-HT), are described by Furshpan et al. (1986),
Matsumoto et al. (in press), and D. Sah and S. G. Matsumoto (unpublished
observations). This paper is concerned with evidence for secretion by these
neurons of norepinephrine (NE) and acetylcholine (ACh). The physiological
effects of the secretion of these two substances onto the myocytes
(excitation and inhibition, respectively) were generally similar to those
reported in vivo. The minimal latencies of the responses were short,
probably due to the high density of innervation. ACh secreted by a neuron
onto itself, at autapses, evoked fast nicotinic EPSPs. We have not detected
autaptic effects attributable to the secretion of NE. A minority of the
neurons were detectably only adrenergic or only cholinergic. The incidence
of these transmitter states was strongly dependent on culture age and
culture conditions; in a heterogeneous group of about 300 reasonably
well-characterized neurons about 17% (12% of neonate-derived) were
apparently purely adrenergic and about 10% (13% of neonate-derived) were
apparently purely cholinergic.(ABSTRACT TRUNCATED AT 400 WORDS)
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