Current injection and receptor-mediated excitation produce similar maximal firing rates in hypoglossal motoneurons

Abstract

The maximum firing rates of motoneurons (MNs), activated in response to synaptic drive, appear to be much lower than that elicited by current injection. It could be that the decrease in input resistance associated with increased synaptic activity (but not current injection) might blunt overall changes in membrane depolarization and thereby limit spike-frequency output. To test this idea, we recorded, in the same cells, maximal firing responses to current injection and to synaptic activation. We prepared 300 μm medullary slices in neonatal rats that contained hypoglossal MNs and used whole-cell patch-clamp electrophysiology to record their maximum firing rates in response to triangular-ramp current injections and to glutamate receptor-mediated excitation. Brief pressure pulses of high-concentration glutamate led to significant depolarization, high firing rates, and temporary cessation of spiking due to spike inactivation. In the same cells, we applied current clamp protocols that approximated the time course of membrane potential change associated with glutamate application and with peak current levels large enough to cause spike inactivation. Means (SD) of maximum firing rates obtained in response to glutamate application were nearly identical to those obtained in response to ramp current injection [glutamate 47.1 ± 12.0 impulses (imp)/s, current injection 47.5 ± 11.2 imp/s], even though input resistance was 40% less during glutamate application compared with current injection. Therefore, these data suggest that the reduction in input resistance associated with receptor-mediated excitation does not, by itself, limit the maximal firing rate responses in MNs.

Keywords: current injection; glutamate; input resistance; motoneuron; spike frequency.

Fig. 1.

Example firing responses in a hypoglossal motoneuron to current injection (A) and glutamate receptor-mediated excitation (B). Firing rate (top), membrane potential (middle), and stimulus protocol (bottom) involving triangular ramp current injection (A) or glutamate (100 mM) application (arrow) to superfusate (B). Dashed, horizontal lines indicate maximum firing rates for 5 spikes immediately before spike inactivation. C: means (SD) of maximum firing rates elicited by current injection and glutamate receptor-mediated excitation. There was no significant difference in firing rates between the 2 conditions. imp/s, impulses per second.

Fig. 2.

Change in input resistance during glutamate application. A: example changes in membrane potential to hyperpolarizing current pulses (50 pA), before and following glutamate application (arrow). TTX was applied to bath to prevent action potentials. Input resistance was estimated by measuring the change in membrane potential, divided by current pulse amplitude. B: means (SD) of input resistance, before and immediately after glutamate application. Overall, input resistance decreased by 40% during receptor-mediated excitation compared with control (*P < 0.05).