The operation of neuronal networks depends on the firing patterns of the network's neurons. When sustained current is injected, some neurons in the central nervous system fire a single action potential and others fire repetitively. For example, in Xenopus laevis tadpoles, primary-sensory Rohon-Beard (RB) neurons fired a single action potential in response to 300-ms rheobase current injections, whereas dorsolateral (DL) interneurons fired repetitively at 10-20 Hz. To investigate the basis for these differences in vivo, we examined drug-induced changes in the firing patterns of Xenopus spinal neurons using whole cell current-clamp recordings. Neuron types were initially separated through cluster analysis, and we compared results produced using different clustering algorithms. We used these results to develop a predictive function to classify subsequently recorded neurons. The potassium channel blocker tetraethylammonium (TEA) converted single-firing RB neurons to low-frequency repetitive firing but reduced the firing frequency of repetitive-firing DL interneurons. Firing frequency in DL interneurons was also reduced by the potassium channel blockers 4-aminopyridine (4-AP), catechol, and margatoxin; 4-AP had the greatest effect. The calcium channel blockers amiloride and nimodipine had few effects on firing in either neuron type but reduced action potential duration in DL interneurons. Muscarine, which blocks M-currents, did not affect RB neurons but reduced firing frequency in DL interneurons. These results suggest that potassium currents may control neuron firing patterns: a TEA-sensitive current prevents repetitive firing in RB neurons, whereas a 4-AP-sensitive current underlies repetitive firing in DL interneurons. The cluster and discriminant analysis described could help to classify neurons in other systems.
Neuron firing patterns underpin the detection and processing of stimuli, influence synaptic interactions, and contribute to the function of networks. To understand how intrinsic membrane properties determine firing patterns, we investigated the biophysical basis of single and repetitive firing in spinal neurons of hatchling Xenopus laevis tadpoles, a well-understood vertebrate model; experiments were conducted in situ. Primary sensory Rohon-Beard (RB) neurons fire singly in response to depolarising current, and dorsolateral (DL) interneurons fire repetitively. RB neurons exhibited a large tetrodotoxin-sensitive sodium current; in DL neurons, the sodium current density was significantly lower. High-voltage-activated calcium currents were similar in both neuron types. There was no evidence of persistent sodium currents, low-voltage-activated calcium currents, or hyperpolarisation-activated currents. In RB neurons, the potassium current was dominated by a tetraethylammonium-sensitive slow component (I(Ks) ); a fast component (I(Kf) ), sensitive to 4-aminopyridine, predominated in DL neurons. Sequential current-clamp and voltage-clamp recordings in individual neurons suggest that high densities of I(Ks) prevent repetitive firing; where I(Ks) is small, I(Kf) density determines the frequency of repetitive firing. Intermediate densities of I(Ks) and I(Kf) allow neurons to fire a few additional spikes on strong depolarisation; this property typifies a novel subset of RB neurons, and may activate escape responses. We discuss how this ensemble of currents and firing patterns underpins the operation of the Xenopus locomotor network, and suggest how simple mechanisms might underlie the similar firing patterns seen in the neurons of diverse species.
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