Abstract

In complex nervous systems patterns of neuronal activity and measures of intrinsic neuronal excitability are often used as criteria for identifying and/or classifying neurons. We asked how well identification of neurons by conventional measures of intrinsic excitability compares with a measure of neuronal excitability derived from a neuron’s behavior in a dynamic clamp constructed two-cell network. We used four cell types from the crab stomatogastric ganglion: the pyloric dilator, lateral pyloric, gastric mill, and dorsal gastric neurons. Each neuron was evaluated for six conventional measures of intrinsic excitability (intrinsic properties, IPs). Additionally, each neuron was coupled by reciprocal inhibitory synapses made with the dynamic clamp to a Morris–Lecar model neuron and the resulting network was assayed for four measures of network activity (network activity properties, NAPs). We searched for linear combinations of IPs that correlated with each NAP, and combinations of NAPs that correlated with each IP. In the process we developed a method to correct for multiple correlations while searching for correlating features. When properly controlled for multiple correlations, four of the IPs were correlated with NAPs, and all four NAPs were correlated with IPs. Neurons were classified into cell types by training a linear classifier on sets of properties, or using k-medoids clustering. The IPs were modestly successful in classifying the neurons, and the NAPs were more successful. Combining the two measures did better than either measure alone, but not well enough to classify neurons with perfect accuracy, thus reiterating that electrophysiological measures of single-cell properties alone are not sufficient for reliable cell identification.

Highlights

  • A major step in elucidating the connectivity of nervous system circuits is identifying the neurons in the circuit

  • We asked how well identification of neurons by conventional measures of intrinsic excitability compares with a measure of neuronal excitability derived from a neuron’s behavior in a dynamic clamp constructed two-cell network

  • Each neuron was coupled by reciprocal inhibitory synapses made with the dynamic clamp to a Morris–Lecar model neuron and the resulting network was assayed for four measures of network activity

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Summary

Introduction

A major step in elucidating the connectivity of nervous system circuits is identifying the neurons in the circuit. In the case of small invertebrate circuits neuronal identification is often straightforward (Getting and Dekin, 1985; Getting, 1989; Marder and Calabrese, 1996; Marder and Bucher, 2001, 2007; Kristan et al, 2005), using a combination of neuronal projection patterns, position, firing patterns, size, and color This has facilitated the establishment of the connectivity diagrams of the circuits underlying stereotyped behaviors in a variety of animals (Mulloney and Selverston, 1974a,b; Selverston et al, 1976; Getting et al, 1980; Selverston and Miller, 1980; Getting, 1981; Hume and Getting, 1982; Hume et al, 1982; Miller and Selverston, 1982a,b; Pearson et al, 1985; Katz, 1996; Marder and Calabrese, 1996; Perrins and Weiss, 1996; Schmidt et al, 2001; Sasaki et al, 2007; Calabrese et al, 2011). Classification of neurons into types and subtypes is not yet routine in larger networks (Jonas et al, 2004; Sugino et al, 2006; Toledo-Rodriguez and Markram, 2007; Miller et al, 2008; Okaty et al, 2011a,b), and a variety of electrophysiological measures are often used to classify neurons in types and subtypes

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