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

Abstract

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.

Correlation of the electrophysiological profiles and sodium channel transcripts of individual rat dorsal root ganglia neurons

“…Potassium and calcium channels also have a major impact on the firing pattern (Deister et al, 2009; Winlove and Roberts, 2012). It is thus possible that the changes we observed were caused by more than one contributing factor (ion channels, pumps, exchangers, etc.).…”

The modulation of two motor behaviors by persistent sodium currents inXenopus laevistadpoles

“…Further RB identification was by their wide action potential and typical firing pattern (Winlove and Roberts 2012) in whole cell recordings. We grouped neurons rhythmically active during fictive swimming as dINs and non-dINs (motoneurons, commissural interneurons, ascending interneurons, repetitive firing descending interneurons), which have similar firing properties to current injections (Li et al 2007a; Sautois et al 2007).…”

“…When the tadpole skin is stimulated repetitively, two types of interneurons are recruited [excitatory commissural interneurons (e-cINs) and repetitive firing descending interneurons (dINrs)], but the dIN activity is suppressed (Li et al 2007b; Li 2015). Tadpole neurons involved in swimming and struggling display different types of firing properties in response to depolarizing current pulses (Li et al 2007a; Li et al 2007b; Sautois et al 2007; Winlove and Roberts 2012). dINs fire a single spike at the onset of depolarizing step currents, whereas other rhythmic neurons show repetitive firing, often with a delay caused by A-type potassium currents (Li 2015).…”

“…dINs fire a single spike at the onset of depolarizing step currents, whereas other rhythmic neurons show repetitive firing, often with a delay caused by A-type potassium currents (Li 2015). The properties of I NaT have been characterized in dissociated tadpole spinal neurons and sensory neurons and sensory interneurons in situ (Dale 1995; Winlove and Roberts 2012). We analyzed sodium currents in the neurons involved in tadpoles swimming and struggling in situ.…”

Slow Wave Activity and Modulations in Mouse Jejunum Myenteric Plexus In Situ

“…Thus, researchers have attempted to access ICC in gut tissue by a recently proposed in situ patch clamping ICC-MY or neurons from longitudinal muscle with myenteric plexus (LMMP) to explore the neural effect on ICC-MY pacemaker activity, under a natural and physiological environment. [9][10][11][12][13] We now report our preliminary data of pacemaker activity and neuronal regulation by using the approach of in situ patch clamp in the myenteric plexus region.…”