Phasic and tonic firing properties in rat oculomotor nucleus motoneurons, studied in vitro

Abstract

Alert-chronic studies show that ocular motoneurons (Mns) exhibit a phasic and tonic firing correlated with eye saccade-velocity and position (fixation), respectively. Differences in the phasic and tonic firing among Mns depend on synaptic inputs and/or the intrinsic membrane properties. We have used in vitro slice preparation to investigate the contribution of membrane properties to firing properties of Wistar rat oculomotor nucleus Mns. We recorded different discharge patterns and focused on Mns with sustained discharge (type I) because they were the most abundant, and their firing pattern resembles that reported in alert preparations. Various differences divided these Mns into types I(A) and I(B); the afterhyperpolarization (AHP) phase of the spike was monophasic in I(A) and biphasic in I(B); I(A) Mns showed tonic or phasic-tonic firing depending on the current intensity, while I(B) Mns showed phasic-tonic discharge; the phasic firing was higher in I(B) than in I(A) Mns; I(A) Mns fired in a narrower range than did I(B) Mns; and I(A) Mns showed lower maximum frequency than did I(B) Mns. In conclusion, I(A) and I(B) Mns show different phasic firing properties and dynamic range, supported by intrinsic membrane properties. We suggest that I(A) and I(B) Mns innervate fast-twitch muscle fibres with different contraction speeds, and could contribute to generating a fine phasic signal for a graded muscle contraction. Finally, we have demonstrated an inverse relationship between Mn thresholds and tonic firing gain, concluding that intrinsic membrane properties could not support the covariation between tonic firing gain and recruitment thresholds reported in alert studies.

Morphology, Intrinsic Membrane Properties, and Rotation-Evoked Responses of Trochlear Motoneurons in the Turtle

“…In a recent report, NietoGonzalez and co-workers were able to categorize ϳ90% of motoneurons in the rat oculomotor nucleus into two groups that bear a strikingly similarity to our type-A and type-B in terms of AHP, spike width, spike frequency adaptation, and dynamic range (Nieto-Gonzalez et al 2007). A nearly identical classification scheme has been applied to neurons in the vestibular nucleus (Serafin et al 1991)-cells that make up the immediate premotor component of the VOR.…”

“…Additionally, study of the VOR involves movement of the head; this compromises the mechanical stability required of intracellular techniques. Intrinsic properties of ocular motoneurons have been investigated in both slice preparations and the intact brain (Baker and Highstein 1975;Baker and Precht 1972; Baker et al 1969a,b; Durand 1989a,b;Goldberg et al 1974Goldberg et al , 1976Grantyn and Grantyn 1978;Gueritaud 1988;Gurahian and Goldberg 1987;Llinas and Baker 1972;Nelson et al 1986;Nieto-Gonzalez et al 2007;Precht and Baker 1972;Russier et al 2003;Shall and Goldberg 1992;Uchino et al 1978). In these studies, synaptic responses were evoked by electrical stimulation of afferent pathways when they were examined at all.…”

Muscarinic Modulation of Recruitment Threshold and Firing Rate in Rat Oculomotor Nucleus Motoneurons

“…We focused our analysis on Mns (n ϭ 54) showing a phasic-tonic discharge in response to suprathreshold current steps (Carrascal et al 2005;Nieto-Gonzalez et al 2007). The carbachol effects (10 M) on the membrane potential and firing frequency for each Mn were quantified before exposure (control condition), during perfusion, and after washout with ACSF.…”

“…Rats were anesthetized with sodium pentobarbital (50 mg kg Ϫ1 ) and quickly decapitated. The methods to obtain the slices, recordings, and analysis are fully detailed elsewhere (Carrascal et al 2006;Nieto-Gonzalez et al 2007). In brief, brain slices of 300 m including the oculomotor nucleus were first incubated in a chamber containing cold sucrose-artificial cerebrospinal fluid (ACSF) for 35-45 min and then transferred to a second chamber containing ACSF at a temperature of 21 Ϯ 1°C.…”

“…For each Mn, the relationship between the steady-state firing frequency and injected current was represented (I-F plot) to calculate the slope, termed I-F gain. We defined current threshold as the intensity of stimulating current capable of eliciting maintained repetitive firing at 20 spikes s Ϫ1 (Nieto-Gonzalez et al 2007). All statistical analyses and exponential fits were carried out on the raw data.…”