The precise timing of presynaptic and postsynaptic activity results in synaptic modifications, which depend on calcium influx. [Ca 2ϩ ] 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 Ca 2ϩ signal during nearcoincident presynaptic and postsynaptic activity. [Ca 2ϩ ] transients evoked by backpropagating

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... ion potentials (bAPs) were mediated by voltage-dependent Ca 2ϩ 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 2ϩ ] transients were restricted to spine heads and were mediated almost entirely by Ca 2ϩ 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 Ca 2ϩ signals in a spine when EPSP and bAP occurred within a time window of ϳ50 msec. Synaptic stimulation, coincident with a bAP, evoked a large postsynaptic Ca 2ϩ 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 Ca 2ϩ influx into synaptically active spines mediated by the brief unblocking of NMDARs during the dendritic bAP.