Abstract
The neuronal input–output function depends on recruitment threshold and gain of the firing frequency–current (f–I) relationship. These two parameters are positively correlated in ocular motoneurons (MNs) recorded in alert preparation and inhibitory inputs could contribute to this correlation. Phasic inhibition mediated by γ-amino butyric acid (GABA) occurs when a high concentration of GABA at the synaptic cleft activates postsynaptic GABAA receptors, allowing neuronal information transfer. In some neuronal populations, low concentrations of GABA activate non-synaptic GABAA receptors and generate a tonic inhibition, which modulates cell excitability. This study determined how ambient GABA concentrations modulate the input–output relationship of rat oculomotor nucleus MNs. Superfusion of brain slices with GABA (100 μm) produced a GABAA receptor-mediated current that reduced the input resistance, increased the recruitment threshold and shifted the f–I relationship rightward without any change in gain. These modifications did not depend on MN size. In absence of exogenous GABA, gabazine (20 μm; antagonist of GABAA receptors) abolished spontaneous inhibitory postsynaptic currents and revealed a tonic current in MNs. Gabazine increased input resistance and decreased recruitment threshold mainly in larger MNs. The f–I relationship shifted to the left, without any change in gain. Gabazine effects were chiefly due to MN tonic inhibition because tonic current amplitude was five-fold greater than phasic. This study demonstrates a tonic inhibition in ocular MNs that modulates cell excitability depending on cell size. We suggest that GABAA tonic inhibition acting concurrently with glutamate receptors activation could reproduce the positive covariation between threshold and gain reported in alert preparation.
Highlights
An individual ocular motoneuron (MN) starts to fire when the position of the eye reaches a certain threshold position in the pulling direction of the muscle that the motoneuron innervates
To determine if the effects on intrinsic membrane properties of high concentrations of GABA and/or the blocking of GABAA receptors by gabazine depended on cell size, we studied the relationship between somatic surface area and input resistance, and between input resistance and rheobase
This study demonstrates that oculomotor nucleus MNs exhibit a tonic inhibitory current in low ambient GABA concentrations
Summary
An individual ocular motoneuron (MN) starts to fire when the position of the eye reaches a certain threshold position in the pulling direction of the muscle that the motoneuron innervates (on-direction). This threshold, MN firing rate increases linearly with eye positions in the on-direction (Fuchs & Luschei, 1970). Neuronal simulation (Dean, 1997; Hazel et al 2002) and ocular MN deafferentation (Pastor & Gonzalez-Forero, 2003) studies support a crucial role of synaptic input in determining the relationship between threshold and gain. Neuronal simulation studies about how a premotor synaptic drive could generate the firing pattern in ocular MNs propose a major role for inhibitory inputs (Hazel et al 2002)
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