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Abteilung Zellphysiologie, Max-Planck-Institut für medizinische Forschung, Heidelberg, Germany. Greg.Stuart@anu.edu.au
1. Initiation and propagation of action potentials evoked by extracellular synaptic stimulation was studied using simultaneous dual and triple patch pipette recordings from different locations on neocortical layer 5 pyramidal neurons in brain slices from 4-week-old rats (P26-30) at physiological temperatures. 2. Simultaneous cell-attached and whole-cell voltage recordings from the apical trunk (up to 700 microns distal to the soma) and the soma indicated that proximal synaptic stimulation (layer 4) initiated action potentials first at the soma, whereas distal stimulation (upper layer 2/3) could initiate dendritic regenerative potentials prior to somatic action potentials following stimulation at higher intensity. 3. Somatic action potentials, once initiated, propagated back into the apical dendrites in a decremented manner which was frequency dependent. The half-width of back propagating action potentials increased and their maximum rate of rise decreased with distance from the soma, with the peak of these action potentials propagating with a conduction velocity of approximately 0.5 m s-1. 4. Back-propagation of action potentials into the dendritic tree was associated with dendritic calcium electrogenesis, which was particularly prominent during bursts of somatic action potentials. 5. When dendritic regenerative potentials were evoked prior to somatic action potentials, the more distal the dendritic recording was made from the soma the longer the time between the onset of the dendritic regenerative potential relative to somatic action potential. This suggested that dendritic regenerative potentials were initiated in the distal apical dendrites, possibly in the apical tuft. 6. At any one stimulus intensity, the initiation of dendritic regenerative potentials prior to somatic action potentials could fluctuate, and was modulated by depolarizing somatic or hyperpolarizing dendritic current injection. 7. Dendritic regenerative potentials could be initiated prior to somatic action potentials by dendritic current injections used to simulate the membrane voltage change that occurs during an EPSP. Initiation of these dendritic potentials was not affected by cadmium (200 microM), but was blocked by TTX (1 microM). 8. Dendritic regenerative potentials in some experiments were initiated in isolated from somatic action potentials. The voltage change at the soma in response to these dendritic regenerative events was small and subthreshold, showing that dendritic regenerative events are strongly attenuated as they spread to the soma. 9. Simultaneous whole-cell recordings from the axon initial segment and the soma indicated that synaptic stimulation always initiated action potentials first in the axon. The further the axonal recording was made from the soma the greater the time delay between axonal and somatic action potentials, indicating a site of action potential initiation in the axon at least 30 microns distal to the soma. 10. Simultaneous whole-cell recordings from the apical dendrite, soma and axon initial segment showed that action potentials were always initiated in the axon prior to the soma, and with the same latency difference, independent of whether dendritic regenerative potentials were initiated or not. 11. It is concluded that both the apical dendrites and the axon of neocortical layer 5 pyramidal neurons in P26-30 animals are capable of initiating regenerative potentials. Regenerative potentials initiated in dendrites, however, are significantly attenuated as they spread to the soma and axon. As a consequence, action potentials are always initiated in the axon before the soma, even when synaptic activation is intense enough to initiate dendritic regenerative potentials. Once initiated, the axonal action potentials are conducted orthogradely into the axonal arbor and retrogradely into the dendritic tree.
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