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The Journal of Neuroscience, December 10, 2003, 23(36):11363-11372
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Behavioral/Systems/Cognitive
Action Potential Initiation and Propagation in Layer 5 Pyramidal Neurons of the Rat Prefrontal Cortex: Absence of Dopamine Modulation
Allan T. Gulledge and
Greg J. Stuart
Division of Neuroscience, John Curtin School of Medical Research, Australian National University, Canberra, ACT 0200, Australia, and Physiology Institute, University of Freiburg, 79104, Freiburg, Germany
Somatic and dendritic whole-cell recording was used to examine action potential (AP) initiation and propagation in layer 5 pyramidal neurons of the rat prelimbic prefrontal cortex. APs generated by somatic current injection, or via antidromic stimulation, were reliably recorded at apical dendritic locations as far as 480 µm from the soma. Although the backpropagation of single APs into the apical dendrite was robust, frequency-dependent attenuation was observed during AP trains delivered at 10-100 Hz. APs were usually initiated close to the soma (presumably in the axon); however, strong depolarizing input to the apical dendrite could generate dendritic spikes that preceded somatic APs. AP backpropagation was dependent solely on activation of dendritic voltage-gated sodium channels and did not require activation of dendritic calcium channels. Despite not playing a role in AP backpropagation, calcium-imaging experiments demonstrated that dendritic calcium channels are activated by backpropagating APs, leading to transient increases in intracellular calcium. In addition, calcium imaging revealed that AP backpropagation into the distal apical tuft was frequency dependent. Finally, we tested whether dopamine, a prominent neuromodulator associated with prefrontal activity, could alter AP initiation or backpropagation. Bath-applied dopamine (10 or 100 µM) did not effect AP backpropagation, frequency-dependent depression, local dendritic spike initiation, or AP-induced calcium signaling. These data indicate that AP backpropagation in prefrontal layer 5 pyramidal neurons is robust but frequency dependent in the distal tuft, requires dendritic sodium rather than calcium channel activation, and, unlike other aspects of neuronal excitability, insensitive to modulation by dopamine.
Key words: prefrontal cortex; apical dendrite; action potential; working memory; dopamine; rat; calcium imaging
Received July 4, 2003;
revised October 13, 2003;
accepted October 14, 2003.
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