The Journal of Neuroscience, February 1, 2000, 20(3):908-918
Secondary Nicotinic Synapses on Sympathetic B Neurons and Their
Putative Role in Ganglionic Amplification of Activity
Paul
Karila and
John P.
Horn
Department of Neurobiology, University of Pittsburgh, School of
Medicine, Pittsburgh, Pennsylvania 15261
The strength and number of nicotinic synapses that converge on
secretomotor B neurons were assessed in the bullfrog by recording intracellularly from isolated preparations of paravertebral sympathetic ganglia 9 and 10. One input to every B neuron invariably produced a
suprathreshold EPSP and was defined as the primary nicotinic synapse.
In addition, 93% of the cells received one to four subthreshold inputs
that were defined as secondary nicotinic synapses. This contradicts the
prevailing view, which has long held that amphibian B neurons are
singly innervated. More important, the results revealed that B cells
provide the simplest possible experimental system for examining the
role of secondary nicotinic synapses on sympathetic neurons. Combining
the convergence data with previous estimates of divergence indicates
that the average preganglionic B neuron forms connections with 50 ganglionic B neurons and that the majority of these nicotinic synapses
are secondary in strength. Secondary EPSPs evoked by low-frequency
stimulation ranged from 0.5 to 10 mV in amplitude and had an average
quantal content of 1. Nonetheless, secondary synapses could trigger
action potentials via four mechanisms: spontaneous fluctuations of EPSP
amplitude, two-pulse facilitation, coactivation with other secondary
synapses, and coactivation with a slow peptidergic EPSP. The data were
used to formulate a stochastic theory of integration, which predicts
that ganglia function as amplifiers of the sympathetic outflow. In this
two-component scheme, primary nicotinic synapses mediate invariant
synaptic gain, and secondary nicotinic synapses mediate
activity-dependent synaptic gain. The model also provides a common
framework for considering how facilitation, metabotropic mechanisms,
and preganglionic oscillators regulate synaptic amplification in
sympathetic ganglia.
Key words:
activity-dependent modulation; bullfrog sympathetic
ganglia; neuronal nicotinic receptors; nicotinic synapses; metabotropic
synapses; synaptic integration; sympathetic nervous system
Copyright © 2000 Society for Neuroscience 0270-6474/00/203908-11$05.00/0
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