Factors influencing motoneuron rhythmic firing: results from a voltage-clamp study

1. The rhythmic firing properties of cat lumbar motoneurons were determined by intracellular injection of constant-current pulses. The activation thresholds of various membrane current components were subsequently determined in the same neurons using the technique of somatic voltage clamp. Voltage steps were employed that traversed the same voltage range as the membrane potential between rhythmic spikes (the "pacemaker potential"). 2. At fast firing rates (e.g., secondary-range firing), the pacemaker potential remains entirely within the range of voltages over which a previously described (42), persistent, inward, calcium current (Ii) is activated during voltage clamp. Thus Ii is tonically activated and counters the repolarizing, outward, potassium currents during fast firing. At slower firing rates (e.g., primary-range firing), the pacemaker potential only partially enters the voltage range where Ii is activated, and this voltage range may not be entered at all the slowest firing rates. Cells in which Ii deteriorated could not be made to fire at fast rates although they could still fire at slow rates. 3. The use of two independent intracellular microelectrodes allowed accurate measurement of the somatic voltage at which spike initiation occurred ("firing level"). In all cells, firing level increased significantly as steady firing rate increased. During a given injected-current pulse, firing level also exhibited a more moderate variation with time. 4. The variation in firing level was caused by the accommodative properties of the axon initial segment. Except at the fastest firing rates, firing level occurs at less depolarized voltages than the somatic sodium conductance threshold. In addition, somatic sodium current shows minimal inactivation over the voltage range traversed by the pacemaker potentials during slower firing rates. An inactivation of about 50% is attained during the maximum firing rate. 5. We discuss the ways by which Ii activation and thr progressive rise in firing level influence motoneuron rhythmic firing. We propose that the basic role of Ii is to aid in maintaining a linear f-I curve, especially at faster firing rates. We hypothesize that the relative balance between persistent inward and outward ionic currents plays a major role in determining the f-I curve slope among different neurons and between primary- and secondary-range firing of cat lumbar motoneurons.