Abstract
Evidence suggests that layer 5 pyramidal neurons can be divided into functional zones with unique afferent connectivity and membrane characteristics that allow for post-synaptic integration of feedforward and feedback inputs. To assess the existence of these zones and their interaction, we characterized the resonance properties of a biophysically-realistic compartmental model of a neocortical layer 5 pyramidal neuron. Consistent with recently published theoretical and empirical findings, our model was configured to have a “hot zone” in distal apical dendrite and apical tuft where both high- and low-threshold Ca2+ ionic conductances had densities 1–2 orders of magnitude higher than anywhere else in the apical dendrite. We simulated injection of broad spectrum sinusoidal currents with linearly increasing frequency to calculate the input impedance of individual compartments, the transfer impedance between the soma and key compartments within the dendritic tree, and a dimensionless term we introduce called resonance quality. We show that input resonance analysis distinguished at least four distinct zones within the model based on properties of their frequency preferences: basal dendrite which displayed little resonance; soma/proximal apical dendrite which displayed resonance at 5–23 Hz, strongest at 5–10 Hz and hyperpolarized/resting membrane potentials; distal apical dendrite which displayed resonance at 8–19 Hz, strongest at 10 Hz and depolarized membrane potentials; and apical tuft which displayed a weak resonance largely between 8 and 10 Hz across a wide range of membrane potentials. Transfer resonance analysis revealed that changes in subthreshold electrical coupling were found to modulate the transfer resonant frequency of signals transmitted from distal apical dendrite and apical tuft to the soma, which would impact the frequencies that individual neurons are expected to respond to and reinforce. Furthermore, eliminating the hot zone was found to reduce amplification of resonance within the model, which contributes to reduced excitability when perisomatic and distal apical regions receive coincident stimulating current injections. These results indicate that the interactions between different functional zones should be considered in a more complete understanding of neuronal integration. Resonance analysis may therefore be a useful tool for assessing the integration of inputs across the entire neuronal membrane.
Highlights
Neocortical architecture facilitates association-based information processing where feedforward and feedback signals connect the many different processing stages of the neocortex
Our results indicate that the frequency preference of proximal apical dendrite and soma is strongest at near resting and hyperpolarized membrane potentials and that, at least in the case of the soma, this is the condition under which signals transmitted to distal apical regions will have the highest transfer resonant impedance, and the largest functional impact on action potential generation
We have shown that tuning of a neuron’s post-synaptic physiological properties to enhance association between distant inputs across the neuronal membrane impacts resonance
Summary
Neocortical architecture facilitates association-based information processing where feedforward and feedback signals connect the many different processing stages of the neocortex. The maximum membrane potential for the soma and basal dendrite compartments was selected based on the peak value of the somatic afterdepolarization potential after the neuron has fired an action potential; the maximum membrane potential for apical dendrite and tuft compartments were selected based on peak membrane potential after local current injection is timed to match the arrival of a back propagated somatic action potential (see Figure 1B, right-top) At each of these membrane potentials, a chirp current was injected into the compartments and we calculated the input impedance by dividing the Fourier spectrum of the resultant membrane potential by the Fourier spectrum of the chirp current, FVm and FI, respectively (Equation 1). The transfer analysis was repeated multiple times, each time with the transfer compartments held at either hyperpolarized, near rest, or various amounts of depolarized membrane potentials using a second DC offset (see Supplementary Materials)
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