Calcium Dynamics in Single Spines during Coincident Pre- and Postsynaptic Activity Depend on Relative Timing of Back-Propagating Action Potentials and Subthreshold Excitatory Postsynaptic Potentials

We compared the transient increase of Ca2+in single spines on basal dendrites of rat neocortical layer 5 pyramidal neurons evoked by subthreshold excitatory postsynaptic potentials (EPSPs) and back-propagating action potentials (APs) by using calcium fluorescence imaging. AP-evoked Ca2+transients were detected in both the spines and in the adjacent dendritic shaft, whereas Ca2+transients evoked by single EPSP2 were largely restricted to a single active spine head. Calcium transients elicited in the active spines by a single AP or EPSP, in spines up to 80 μ m for the soma, were of comparable amplitude. The Ca2+transient in an active spine evoked by pairing an EPSP and a back-propagating AP separated by a time interval of 50 ms was larger if the AP followed the EPSP than if it preceded it. This difference reflected supra- and sublinear summation of Ca2+transients, respectively. A comparable dependence of spinous Ca2+transients on relative timing was observed also when short bursts of APs and EPSPs were paired. These results indicate that the amplitude of the spinous Ca2+transients during coincident pre- and postsynaptic activity depended critically on the relative order of subthreshold EPSPs and back-propagating APs. Thus, in neocortical neurons the amplitude of spinous Ca2+transients could encode small time differences between pre- and postsynaptic activity.