The firing patterns of spinal neurons: in situ patch‐clamp recordings reveal a key role for potassium currents

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.