Secondary Nicotinic Synapses on Sympathetic B Neurons and Their Putative Role in Ganglionic Amplification of Activity

Abstract

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.

Functional organization of vasodilator neurons in pelvic ganglia of female guinea pigs: Comparison with uterine motor neurons

“…They may integrate multiple synaptic inputs from preganglionic and other peripheral neurons (Szurszewski, 1981;McLachlan and Meckler, 1989;de Groat and Booth, 1993a b;Felix et al, 1998), they may act as low-pass filters of preganglionic activity (Undem and Myers, 1997), or they can operate as spatial amplifiers of the central command (Karila and Horn, 2000). How a particular postganglionic neuron integrates and modifies information is determined by a combination of its morphology, which is related to the number of its synaptic inputs (Purves and Hume, 1981;Gibbins et al, 2000) and its expression of a suite of ionic (mainly potassium) conductances (Adams and Harper, 1995;Myers, 1998).…”

Age‐associated synapse elimination in mouse parasympathetic ganglia

“…These occasional small potentials indicate that, as previously seen in rat (Lichtman, 1980), mouse SMG cells are sometimes innervated by additional subthreshold inputs in addition to one primary input. The functional significance of these weak additional inputs is not understood (e.g., Karila and Horn, 2000). The amplitudes of the suprathreshold EPSPs were measured by timing them to occur in the refractory period of a directly elicited action potential as has been done previously (e.g., Purves, 1975) [ Fig.…”

Structure of peripheral synapses: autonomic ganglia

“…Thus, ganglia also provide a site for the final integration of the neural pathways regulating visceral activity (e.g. Karila and Horn 2000).…”

“…Morphological studies dating back more than a hundred years together with more recent functional experiments have shown that these neurons usually receive a single dominant preganglionic input, although some exceptions to this have been reported (e.g. Dennis and Sargent 1978;Karila and Horn 2000).…”