P. Karila et Jp. Horn, Secondary nicotinic synapses on sympathetic B neurons and their putative role in ganglionic amplification of activity, J NEUROSC, 20(3), 2000, pp. 908-918
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 in
put to every B neuron invariably produced a suprathreshold EPSP and was def
ined as the primary nicotinic synapse. In addition, 93% of the cells receiv
ed one to four subthreshold inputs that were defined as secondary nicotinic
synapses. This contradicts the prevailing view, which has long held that a
mphibian B neurons are singly innervated. More important, the results revea
led that B cells provide the simplest possible experimental system for exam
ining the role of secondary nicotinic synapses on sympathetic neurons. Comb
ining the convergence data with previous estimates of divergence indicates
that the average preganglionic B neuron forms connections with 50 ganglioni
c B neurons and that the majority of these nicotinic synapses are secondary
in strength. Secondary EPSPs evoked by low-frequency stimulation ranged fr
om 0.5 to 10 mV in amplitude and had an average quantal content of 1. Nonet
heless, secondary synapses could trigger action potentials via four mechani
sms: spontaneous fluctuations of EPSP amplitude, two-pulse facilitation, co
activation with other secondary synapses, and coactivation with a slow pept
idergic EPSP. The data were used to formulate a stochastic theory of integr
ation, which predicts that ganglia function as amplifiers of the sympatheti
c 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 co
nsidering how facilitation, metabotropic mechanisms, and preganglionic osci
llators regulate synaptic amplification in sympathetic ganglia.