Electrotonic coupling between rat sympathetic preganglionic neurones in vitro.

Abstract

1. Using the whole-cell recording technique in rat spinal cord slices we have shown that 26 % of sympathetic preganglionic neurones (SPNs) show spontaneous membrane potential oscillations. These oscillations consist of trains of biphasic waves, which we have termed spikelets because of their similarity to truncated action potentials. 2. The spikelets were inhibited by TTX and anaesthetics such as a-chloralose but not by the intracellular application of lidocaine N-ethyl bromide (QX-314). 3. By stimulating the ventral roots we have demonstrated the presence of short-latency depolarizations (SLDs) in oscillating neurones. These SLDs have a similar waveform to the spontaneous spikelets, and also show the ability to override the frequency of occurrence of the spontaneous spikelets. These observations suggest that the spikelets result from electrotonic coupling between the oscillating SPNs. 4. SLDs were also observed in a population of non-oscillating, electrotonically coupled, quiescent SPNs. It was possible to induce oscillations in these neurones by the injection of depolarizing current (in the presence of QX-314), suggesting that these neurones are also gap-junction coupled. 5. Simultaneous whole-cell recordings were obtained from twenty-three pairs of SPNs. Two pairs displayed both spontaneous, synchronized oscillations and action potentials. Electrotonic coupling was confirmed by the detection of membrane polarization in both neurones in response to current injected into one neurone. In a further two pairs of quiescent SPNs, injection of depolarizing current pulses into one neurone induced action potential discharge in that neurone and a depolarization and oscillations in the other neurone. 6. The ability of groups of electrotonically coupled SPNs to generate spontaneous discharges within the spinal cord provides a novel mechanism for the integration and synchronization of information within the sympathetic nervous system.

Voltage-Dependent Enhancement of Electrical Coupling by a Subthreshold Sodium Current

“…This finding was confirmed by performing simultaneous extracellular recordings of the M-cell antidromic spike during QX-314 injections (data not shown). Thus, although the diffusion of small or ineffective amounts of QX-314 to the M-cells cannot be ruled out, our data are consistent with previous reports (Logan et al, 1996;Mann-Metzer and Yarom, 1999) indicating that QX-314 is impermeable through neuronal gap junctions.…”

Electrical Coupling between Locomotor-Related Excitatory Interneurons in the Mammalian Spinal Cord

“…Electrical transmission has been reported previously between somatic (Walton and Navarrete, 1991;Chang et al, 1999) and sympathetic (Logan et al, 1996) motoneurons in the rat spinal cord. However, to the best of our knowledge, this is the first report that demonstrates a high-incidence electrical transmission between excitatory, locomotor-related interneurons in the mammalian spinal cord.…”

Electrophysiological properties of electrical synapses between rat sympathetic preganglionic neurones in vitro

“…If the ePSPs were conducted passively through an intermediate neurone, occasional recordings of spontaneous or antidromically evoked electrotonically mediated membrane potential oscillations with considerably larger amplitudes and faster kinetics than ePSPs between pairs of SPNs would be expected, but have not been observed (cf. Spanswick & Logan, 1990;Logan et al 1996). The ePSPs characterised were also unlikely to result from a mixture of monosynaptic and passively conducted polysynaptic inputs, as there was no significant relationship between their amplitude and rise times, which would otherwise be expected from the resulting variability in the Sympathetic preganglionic electrical synapses J. Physiol.…”

“…Recordings were made simultaneously from pairs of neurones in current-clamp mode. SPNs were identified by their characteristic electrophysiological properties (Pickering et al 1991;Logan et al 1996). Electrotonic coupling between neurones was detected by observation of a membrane potential change in one neurone following a membrane polarisation induced by injection of current into the other neurone.…”

“…Electrophysiological recordings were made from transverse thoracolumbar spinal cord slices as described previously (Pickering et al 1991;Logan et al 1996). Sprague-Dawley rats, aged 8-14 days, were anaesthetised with Enflurane (7 % in Oµ; Abbott laboratories, Kent, UK), killed by decapitation and the spinal cord removed and cut into slices (300-500 ìm thick) using a vibratome (Intracel Series 1000, Royston, UK).…”