Single Spine Ca2+ Signals Evoked by Coincident EPSPs and Backpropagating Action Potentials in Spiny Stellate Cells of Layer 4 in the Juvenile Rat Somatosensory Barrel Cortex

Abstract

The precise timing of presynaptic and postsynaptic activity results in synaptic modifications, which depend on calcium influx. [Ca2+] transients in the spines of spiny neurons in layer 4 (L4) of the somatosensory barrel cortex of young rats were investigated in thalamocortical brain slices by two-photon excitation microscopy to determine the spike timing dependence of the Ca2+ signal during near-coincident presynaptic and postsynaptic activity. [Ca2+] transients evoked by backpropagating action potentials (bAPs) were mediated by voltage-dependent Ca2+ channels and were of comparable size in a spine and adjacent dendritic shaft. They decreased with the distance of the spine from the soma. EPSP-evoked [Ca 2+] transients were restricted to spine heads and were mediated almost entirely by Ca2+ influx through NMDA receptors (NMDARs). Their amplitude was independent of the position of the spine along the dendritic arbor. bAPs interacted with EPSPs to generate sublinear or supralinear Ca2+ signals in a spine when EPSP and bAP occurred within a time window of ∼50 msec. Synaptic stimulation, coincident with a bAP, evoked a large postsynaptic Ca2+ influx that was restricted to a single spine, even after EPSPs were blocked by the AMPA receptor antagonist NBQX that rendered synapses effectively "electrically silent." We conclude that the spines of L4 cells can act as sharply tuned detectors for patterns of APs occurring in the boutons of the afferents to L4 cells and the spines of L4 cell dendrites. The readout for near-coincident presynaptic and postsynaptic APs is a large transient Ca2+ influx into synaptically active spines mediated by the brief unblocking of NMDARs during the dendritic bAP.