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Maturation of layer 5 neocortical pyramidal neurons: amplifying salient layer 1 and layer 4 inputs by Ca²⁺ action potentials in adult rat tuft dendrites

J. Julius Zhu

1. Changes in the arborization and electrical excitability of the apical dendritic tufts of pyramidal cells of cortical layer 5 were examined during the first 2 months (postnatal days (P)2-56) of postnatal development in rats.

2. Reconstructions of biocytin-filled neurons showed that the apical dendritic trunk was continually growing, becoming longer and thicker and that the distance between the tuft and soma increased more than 5-fold.

3. In P2 animals, both the tuft and soma had a high input resistance (> 500 M) and the tuft was electrotonically close to the soma. In contrast, the apical tuft and soma of P56 neurons had a low input resistance (< 50 M) and they were electrotonically isolated from each other.

4. Depolarizing current pulses injected into the tuft of P2 cells generated mostly Na⁺-dependent regenerative dendritic potentials of short duration (~15 ms) while in the tuft of P56 animals, complex regenerative potentials were generated which had a longer duration (~55 ms) and were Na⁺ and Ca²⁺ dependent. In young and juvenile animals (P14-28) dendritic regenerative potentials could be restricted to the apical dendritic tuft whereas in adult animals (> P42), the complex regenerative potentials frequently occurred simultaneously with somatic action potentials.

5. The main developmental change in layer 5 pyramidal neurons, as assayed with square pulse current injections and synaptic stimulations, is the progressive electrotonic isolation of the dendritic tuft from the soma. This change is concomitant with the appearance of complex, mostly Na⁺- and Ca²⁺-dependent, regenerative dendritic potentials initiated partly in the tuft and partly in the axon. The coupling of the dendritic tuft and axonal initiation zones for regenerative potentials by active dendritic Na⁺ and Ca²⁺ conductances enables mature layer 5 pyramidal neurons to detect selectively the salient distal synaptic inputs and coincident synaptic inputs arriving at different cortical layers.

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