Abstract
Spinal motoneurons may display a variety of firing patterns including bistability between repetitive firing and quiescence and, more rarely, bistability between two firing states of different frequencies. It was suggested in the past that firing bistability required that the persistent L-type calcium current be segregated in distal dendrites, far away from the spike generating currents. However, this is not supported by more recent data. Using a two compartment model of motoneuron, we show that the different firing patterns may also result from the competition between the more proximal dendritic component of the dendritic L-type conductance and the calcium sensitive potassium conductance responsible for afterhypolarization (AHP). Further emphasizing this point, firing bistability may be also achieved when the L-type current is put in the somatic compartment. However, this requires that the calcium-sensitive potassium conductance be triggered solely by the high threshold calcium currents activated during spikes and not by calcium influx through the L-type current. This prediction was validated by dynamic clamp experiments in vivo in lumbar motoneurons of deeply anesthetized cats in which an artificial L-type current was added at the soma. Altogether, our results suggest that the dynamical interaction between the L-type and afterhyperpolarization currents is as fundamental as the segregation of the calcium L-type current in dendrites for controlling the discharge of motoneurons.
Highlights
The discovery of a L-type calcium current in the dendrites of motoneurons (Schwindt and Crill, 1984; Hounsgaard and Kiehn, 1985) greatly changed our vision of their excitability properties
OF RESULTS We studied a model of motoneuron where the somatic and the dendritic compartments are 10 times more strongly coupled than in the BRK model
We demonstrated that the dynamical competition between the dendritic calcium L-type current and the somatic AHP current may lead to graded firing, quiescence/firing bistability below recruitment, or firing bistability, depending on the balance between these two currents
Summary
The discovery of a L-type calcium current in the dendrites of motoneurons (Schwindt and Crill, 1984; Hounsgaard and Kiehn, 1985) greatly changed our vision of their excitability properties. Passive voltage attenuation from soma to dendrites reaches 70% in this model, which would correspond to a distance from the soma of 1.2 times the space constant λ in an equivalent cable This does not fit with later immunocytochemical and modeling studies (Simon et al, 2003; Elbasiouny et al, 2005, 2006; Ballou et al, 2006; Bui et al, 2006; Zhang et al, 2006; Grande et al, 2007; Zhang et al, 2008), which suggest that the L-type current is closer to the soma (0.6 ± 0.2 λ) and displays a smaller somatic component. This more proximal location allows the somatic afterhyperpolarization (AHP) following spikes to deactivate the L-type current. Elbasiouny et al (2006) pointed out that the AHP could enable graded activation of that current in response to synaptic excitation of the dendrites
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