On the Number of Preganglionic Neurons Driving Human Postganglionic Sympathetic Neurons: A Comparison of Modeling and Empirical Data

Vaughan G Macefield

doi:10.3389/fnins.2011.00132

Abstract

Postganglionic sympathetic axons in awake healthy human subjects, regardless of their identity as muscle vasoconstrictor, cutaneous vasoconstrictor, or sudomotor neurons, discharge with a low firing probability (∼30%), generate low firing rates (∼0.5 Hz) and typically fire only once per cardiac interval. The purpose of the present study was to use modeling of spike trains in an attempt to define the number of preganglionic neurons that drive an individual postganglionic neuron. Artificial spike trains were generated in 1–3 preganglionic neurons converging onto a single postganglionic neuron. Each preganglionic input fired with a mean interval distribution of either 1000, 1500, 2000, 2500, or 3000 ms and the SD varied between 0.5×, 1.0×, and 2.0× the mean interval; the discharge frequency of each preganglionic neuron exhibited positive skewness and kurtosis. Of the 45 patterns examined, the mean discharge properties of the postganglionic neuron could only be explained by it being driven by, on average, two preganglionic neurons firing with a mean interspike interval of 2500 ms and SD of 5000 ms. The mean firing rate resulting from this pattern was 0.22 Hz, comparable to that of spontaneously active muscle vasoconstrictor neurons in healthy subjects (0.40 Hz). Likewise, the distribution of the number of spikes per cardiac interval was similar between the modeled and actual data: 0 spikes (69.5 vs 66.6%), 1 spike (25.6 vs 21.2%), 2 spikes (4.3 vs 6.4%), 3 spikes (0.5 vs 1.7%), and 4 spikes (0.1 vs 0.7%). Although some features of the firing patterns could be explained by the postganglionic neuron being driven by a single preganglionic neuron, none of the emulated firing patterns generated by the firing of three preganglionic neurons matched the discharge of the real neurons. These modeling data indicate that, on average, human postganglionic sympathetic neurons are driven by two preganglionic inputs.

Highlights

Microelectrode recordings from peripheral nerves of awake human subjects have revealed common features in their discharge patterns of individual postganglionic sympathetic axons, including a probabilistic firing pattern, a tendency to fire only one spike per cardiac interval, an exponential distribution of instantaneous frequencies, and low mean firing rate (∼0.5 Hz)
We have argued previously, based on a comparison of the firing properties of postganglionic sympathetic neurons and alpha motoneurons, that the duration of a sympathetic burst would limit the number of times a neuron can fire (Macefield and Elam, 2004), but we cannot escape the fact that the firing pattern is determined by the level of synaptic drive a given postganglionic neuron receives
Using a variety of model spike train patterns, attempts were made to model the discharge of individual muscle vasoconstrictor neurons by combining the stochastic firing patterns of one to three input neurons converging onto a single output neuron

Summary

Introduction

Microelectrode recordings from peripheral nerves of awake human subjects have revealed common features in their discharge patterns of individual postganglionic sympathetic axons, including a probabilistic firing pattern, a tendency to fire only one spike per cardiac interval, an exponential distribution of instantaneous frequencies, and low mean firing rate (∼0.5 Hz) These features are shared across the unit types that have so far been studied: muscle vasoconstrictor (Macefield et al, 1994; Macefield and Wallin, 1999a), cutaneous vasoconstrictor (Macefield and Wallin, 1999b), and sudomotor (Macefield and Wallin, 1996) neurons in healthy subjects (for review see Macefield et al, 2002). We have argued previously, based on a comparison of the firing properties of postganglionic sympathetic neurons and alpha motoneurons, that the duration of a sympathetic burst would limit the number of times a neuron can fire (Macefield and Elam, 2004), but we cannot escape the fact that the firing pattern is determined by the level of synaptic drive a given postganglionic neuron receives.

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