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.

Inhibition linearizes firing rate responses in human motor units: implications for the role of persistent inward currents

“…Accordingly, we compared, in the same MNs, maximal firing rates evoked by somatic current injection to that elicited by extracellular micro‐ejection of high concentration glutamate (Wakefield et al . ). Despite substantial reduction in input resistance associated with opening of ligand‐gated channels during glutamate application, the maximal firing rates achieved through the two methods were not different from one another.…”

“…We next investigated the possibility that a progressive reduction in cell input resistance associated with increased synaptic activity (but not during current injection) might limit the ability of MNs to increase firing rates to high levels. Accordingly, we compared, in the same MNs, maximal firing rates evoked by somatic current injection to that elicited by extracellular micro-ejection of high concentration glutamate (Wakefield et al 2016). Despite substantial reduction in input resistance associated with opening of ligand-gated channels during glutamate application, the maximal firing rates achieved through the two methods were not different from one another.…”