Glutamate modulates the firing rate in oculomotor nucleus motoneurons as a function of the recruitment threshold current

Abstract

Key points• This study deals with the cellular mechanisms involved in firing rate modulation in vivo in the oculomotor system where there are requirements for high firing rates by motoneurons.• The study demonstrates that glutamate effects depend on the recruitment threshold and, presumably, motoneuron size.• Mid-and high-threshold motoneurons in response to glutamate decrease their voltage threshold and strengthened the tonic and phasic components of the firing rate.• In a functional context, motoneurons could be recruited at lower recruitment threshold and could generate a strong muscle contraction under glutamate modulation to perform saccadic eye movements with different velocities and/or to maintain the eye in different eccentric positions in the orbit.• Our results suggest that the recruitment and firing behaviour of ocular motoneurons can be modified in vivo by glutamatergic synaptic inputs. It provides a link between cellular function and behavioural motoneuron output.Abstract Studies in alert preparations have demonstrated that ocular motoneurons exhibit a phasic-tonic firing rate related to eye velocity and position, respectively. The slopes of these relationships are higher in motoneurons with higher recruitment threshold and have been proposed to depend upon synaptic input. To investigate this hypothesis, motoneurons of the rat oculomotor nucleus were recorded in a brain slice preparation in control conditions and during glutamate (5 μM) application to the bath. Glutamate did not affect membrane potential or input resistance, but produced a decrease in rheobase and depolarization voltage as a function of the current needed for generating a maintained repetitive discharge (recruitment threshold current). In addition, glutamate compressed the range of recruitment threshold current (0.1-0.4 nA) as compared to the control (0.15-0.7 nA). Glutamate exposed motoneurons showed an increase in the tonic frequency gain and the peak frequency. Such increments depended on the recruitment threshold current and the last recruited motoneurons almost doubled the tonic frequency gain (35.2 vs. 57.9 spikes s −1 nA −1 ) and the peak frequency (52.4 vs. 102.6 spikes s −1 ). Finally, glutamate increased the spike frequency adaptation due to a significant increase in the phasic firing component as compared to the tonic one. In conclusion, glutamate modulates tonic and phasic discharge properties as a function of the recruitment threshold current and, presumably, motoneuron size. These findings contribute to understand the link between cellular functions and motoneuron discharge during oculomotor behaviour.

Transmitter inputs to different motoneuron subgroups in the oculomotor and trochlear nucleus in monkey

“…This may indicate that SIF motoneurons participate in the fast and slow components of the postsynaptic response to glutamate. This is in line with in vitro studies on rat oculomotor neurons showing that smaller motoneurons with low-recruitment threshold currents have higher input resistances and exhibit tonic firing—as assumed for MIF motoneurons and whose firing pattern remains essentially unmodified by glutamate application (Torres-Torrelo et al, 2012 ). The phasic-tonic firing of larger motoneurons—such as SIF motoneurons—with lower input resistances and with high recruitment threshold currents, is strengthened by glutamate and could provide strong muscle contractions for (saccadic) eye movements (Torres-Torrelo et al, 2012 ).…”

“…Transmitter inputs may not only convey a specific postsynaptic reponse, but may modulate the excitability of the motoneurons, for example by opening chloride channels conveyed by GABA and glycine (Lorenzo et al, 2007 ). Recent in vivo studies in rat demonstrated that the firing properties of motoneurons in nIII (tonic and phasic discharge) as function of recruitment threshold current and cell size can be modified by glutamatergic input (Torres-Torrelo et al, 2012 ). Based on their findings from in vitro studies of rat nIII motoneurons superfused with GABA, the authors propose that motoneuron firing rates are essentially driven by transient neurotransmission of different transmitters.…”

Gaze-Stabilizing Central Vestibular Neurons Project Asymmetrically to Extraocular Motoneuron Pools

“…One input spike had a value of 1; after convolution, a threshold of 1.8 was reached if at least four spikes were present across all inputs over a 4 ms period. Changing the threshold ensured that the postsynaptic response would not saturate as the number of inputs increased; the specific threshold did not change the relationships we observed and is expected from the basic properties of extraocular motoneurons ( Torres-Torrelo et al, 2012 ). We generated 80 distinct spike trains, reflecting the number of motoneurons in a given motoneuron pool ( Greaney et al, 2017 ).…”

Gaze-stabilizing central vestibular neurons project asymmetrically to extraocular motoneuron pools

“…One input spike had a value of 1; after convolution, a threshold of 1.8 was reached if at least four spikes were present across all inputs over a 4ms period. Changing the threshold ensured that the post-synaptic response would not saturate as the number of inputs increased; the specific threshold did not change the relationships we observed and is expected from the basic properties of extraocular motoneurons (Torres-Torrelo et al, 2012). We generated 80 distinct spike trains, reflecting the number of motoneurons in a given motoneuron pool (Greaney et al, 2016).…”