Axonal Speeding: Shaping Synaptic Potentials in Small Neurons by the Axonal Membrane Compartment

Abstract

The role of the axonal membrane compartment in synaptic integration is usually neglected. We show here that in interneurons of the cerebellar molecular layer, where dendrites are so short that the somatodendritic domain can be considered isopotential, the axonal membrane contributes a significant part of the cell input capacitance. We examine the impact of axonal membrane on synaptic integration by cutting the axon with two-photon illumination. We find that the axonal compartment acts as a sink for signals generated at fast conductance synapses, thus increasing the initial decay rate of corresponding synaptic potentials over the value predicted from the resistance-capacitance (RC) product of the cell membrane; signals generated at slower synapses are much less affected. This mechanism sharpens the spike firing precision of fast glutamatergic inputs without resorting to multisynaptic pathways.

Impact of single-site axonal GABAergic synaptic events on cerebellar interneuron activity

“…Even though in current clamp the voltage changes are presumably shunted by the activation of the autoRs and the subsequent activation of the Na v conductance, the amplification produced by the latter seems to prevail and prolongs D 37 . At the same time, the axonal space constant () estimated by computational simulation was 434 µm (not depicted), consistent with previous estimates (Pouzat and Marty, 1999;Mejia-Gervacio et al, 2007). The difference between these two values may be caused by: (a) the shunting effect produced by the activation of the autoRs and the Na v channels and (b) the low-pass filtering effect of the axonal membrane, which affects fast synaptic signals, whereas the spatial constant AutoR-mediated responses are amplified by Na v conductances Some of the results obtained so far suggest that the autoR-mediated depolarizations are not exclusively passive, but involve an active mechanism: first, the finding that ASPs are capable of triggering APs; second, the lack of negative correlation between  rise and ASP amplitude ( Fig.…”

“…The difference between these two values may be caused by: (a) the shunting effect produced by the activation of the autoRs and the Na v channels and (b) the low-pass filtering effect of the axonal membrane, which affects fast synaptic signals, whereas the spatial constant AutoR-mediated responses are amplified by Na v conductances Some of the results obtained so far suggest that the autoR-mediated depolarizations are not exclusively passive, but involve an active mechanism: first, the finding that ASPs are capable of triggering APs; second, the lack of negative correlation between  rise and ASP amplitude ( Fig. 6 D); third, the fact that  decay of ASPs is systematically longer than 32 ms, the membrane time constant that has been calculated for MLIs (Mejia-Gervacio et al, 2007); and last, the longer D 37 in current clamp (Fig. 6 C) compared with the one in voltage clamp (Fig.…”

“…Values for the biophysical parameters included in the model were taken from previously validated models (Pouzat and Marty, 1999;Mejia-Gervacio et al, 2007). The model comprised two connected, cylindrical compartments: one corresponding to the soma and dendrites (10-µm length × 10-µm diameter), and the other one to the axon (200-µm length × 0.5-µm diameter).…”

Distinct nonuniform cable properties optimize rapid and efficient activation of fast-spiking GABAergic interneurons

“…Furthermore, the axonal arborization was not included in any of these studies, and a possible nonuniformity of R m was not considered (27, 28). However, complete passive cable models will be necessary for understanding the mechanisms of both dendritic integration and action potential initiation in GABAergic interneurons (13,29).To address these questions, we developed detailed passive cable models (27,28,(30)(31)(32) of BCs in the dentate gyrus. To obtain accurate measurement of R i and somatodendritic nonuniformity of R m , both dual somatic and somatodendritic recordings were performed.…”

“…Furthermore, the axonal arborization was not included in any of these studies, and a possible nonuniformity of R m was not considered (27, 28). However, complete passive cable models will be necessary for understanding the mechanisms of both dendritic integration and action potential initiation in GABAergic interneurons (13,29).…”