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Dendritic Properties of Turtle Pyramidal Neurons

¹Department of Physiology, University of Bern, Bern, Switzerland; ²Department of Physiology, New York Medical College, Valhalla, New York; ³Evolved Machines, Palo Alto, California; and ⁴Marine Biological Laboratory, Woods Hole, Massachusetts

Submitted 27 September 2007; accepted in final form 27 November 2007

The six-layered mammalian neocortex evolved from the three-layered paleocortex, which is retained in present-day reptiles such as the turtle. Thus the turtle offers an opportunity to examine which cellular and circuit properties are fundamental to cortical function. We characterized the dendritic properties of pyramidal neurons in different cortical regions of mature turtles, Pseudemys scripta elegans, using whole cell recordings and calcium imaging from the axon, soma, and dendrites in a slice preparation. The firing properties, in response to intrasomatic depolarization, resembled those previously recorded with sharp electrodes in this preparation. Somatic spikes led to active backpropagating high-amplitude dendritic action potentials and intracellular calcium ion concentration ([Ca²⁺]_i) changes at all dendritic locations, suggesting that both backpropagation and dendritic voltage-gated Ca²⁺ channels are primitive traits. We found no indication that Ca²⁺ spikes could be evoked in the dendrites, but fast Na⁺ spikes could be initiated there following intradendritic stimulation. Several lines of evidence indicate that fast, smaller-amplitude somatic spikes ("prepotentials") that are easily recorded in this preparation are generated in the axon. Most synaptically activated [Ca²⁺]_i changes resulted from Ca²⁺ entry through voltage-gated channels. In some cells synaptic stimulation evoked a delayed Ca²⁺ wave due to release from internal stores following activation of metabotropic glutamate receptors. With some small differences these properties resemble those of pyramidal neurons in mammalian species. We conclude that spike backpropagation, dendritic Ca²⁺ channels, and synaptically activated Ca²⁺ release are primitive and conserved features of cortical pyramidal cells, and therefore likely fundamental to cortical function.

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