Dendritic Properties of Turtle Pyramidal Neurons

Abstract

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.

Properties of Layer 6 Pyramidal Neuron Apical Dendrites

“…This might indicate that the point of failure for effective backpropagation in L6 pyramidal neuron is close enough to the soma that somatic depolarization can influence it. A similar anomalous increase was observed in rat olfactory cortical and turtle cortex pyramidal neurons (Larkum et al, 2008;Bathellier et al, 2009).…”

Dendritic Compartment and Neuronal Output Mode Determine Pathway-Specific Long-Term Potentiation in the Piriform Cortex

“…In layer 2 pyramidal cells of the piriform cortex, we did not observe such a regenerative mechanism, which is comparable with the CA1 pyramidal cell in the hippocampus (for review, see Sjöström et al, 2008). It is tempting to speculate that the palaeocortex, like its phylogenetic relative, the threelayered amphibian cortex in the turtle (Larkum et al, 2008), does not use supralinear Ca 2ϩ spikes for dendritic signal integration. This would render AP burst-mediated Ca 2ϩ spikes an evolutionary younger mechanism, which is an exclusive property of the neocortex.…”

Cortical Evolution: Introduction to the Reptilian Cortex

“…Although they are embedded in the same basic connectivity scheme, semilunar and superficial pyramidal cells receive different ratios of afferent to associational inputs and may therefore belong to distinct functional sub-circuits (Suzuki and Bekkers 2011; but see Poo and Isaacson 2011), consistent with morphological differences between their dendritic trees and their laminar position (Wiegand et al 2011). Although data on subpopulations of principal cells in DCx are few, analysis of Golgi-stained material also revealed different morphological classes of spiny neurons at different laminar and sublaminar positions in reptilian cortex (Ulinski 1977;Desan 1984) PCx and DCx pyramidal neurons are also similar with respect to their dendritic electrophysiological properties, suggesting comparable integrative properties at the subcellular level (Larkum et al 2008;Bathellier et al 2009). Different subtypes of inhibitory interneurons have been identified in PCx based on molecular markers, the morphology of their dendritic arbor and the distribution of their axonal projections (reviewed in Suzuki and Bekkers 2007).…”