Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons

Abstract

Simultaneous whole‐cell voltage and Ca 2+ fluorescence measurements were made from the distal apical dendrites and the soma of thick tufted pyramidal neurons in layer 5 of 4‐week‐old (P28–32) rat neocortex slices to investigate whether activation of distal synaptic inputs can initiate regenerative responses in dendrites. Dual whole‐cell voltage recordings from the distal apical trunk and primary tuft branches (540–940 μ m distal to the soma) showed that distal synaptic stimulation (upper layer 2) evoking a subthreshold depolarization at the soma could initiate regenerative potentials in distal branches of the apical tuft which were either graded or all‐or‐none. These regenerative potentials did not propagate actively to the soma and axon. Calcium fluorescence measurements along the apical dendrites indicated that the regenerative potentials were associated with a transient increase in the concentration of intracellular free calcium ([Ca 2+]i) restricted to distal dendrites. Cadmium added to the bath solution blocked both the all‐or‐none dendritic regenerative potentials and local dendritic [Ca 2+]i transients evoked by distal dendritic current injection. Thus, the regenerative potentials in distal dendrites represent local Ca 2+ action potentials. Initiation of distal Ca 2+ action potentials by a synaptic stimulus required coactivation of AMPA‐ and NMDA‐type glutamate receptor channels. It is concluded that in neocortical layer 5 pyramidal neurons of P28–32 animals glutamatergic synaptic inputs to the distal apical dendrites can be amplified via local Ca 2+ action potentials which do not reach threshold for axonal AP initiation. As amplification of distal excitatory synaptic input is associated with a localized increase in [Ca 2+]i these Ca 2+ action potentials could control the synaptic efficacy of the distal cortico‐cortical inputs to layer 5 pyramidal neurons.