Somatic versus dendritic resonance: differential filtering of inputs through non-uniform distributions of active conductances

PLoS One. 2013 Nov 5;8(11):e78908. doi: 10.1371/journal.pone.0078908. eCollection 2013.

Abstract

Synaptic inputs to neurons are processed in a frequency-dependent manner, with either low-pass or resonant response characteristics. These types of filtering play a key role in the frequency-specific information flow in neuronal networks. While the generation of resonance by specific ionic conductances is well investigated, less attention has been paid to the spatial distribution of the resonance-generating conductances across a neuron. In pyramidal neurons - one of the major excitatory cell-types in the mammalian brain - a steep gradient of resonance-generating h-conductances with a 60-fold increase towards distal dendrites has been demonstrated experimentally. Because the dendritic trees of these cells are large, spatial compartmentalization of resonant properties can be expected. Here, we use mathematical descriptions of spatially extended neurons to investigate the consequences of such a distal, dendritic localization of h-conductances for signal processing. While neurons with short dendrites do not exhibit a pronounced compartmentalization of resonance, i.e. the filter properties of dendrites and soma are similar, we find that neurons with longer dendrites ([Formula: see text] space constant) can show distinct filtering of dendritic and somatic inputs due to electrotonic segregation. Moreover, we show that for such neurons, experimental classification as resonant versus nonresonant can be misleading when based on somatic recordings, because for these morphologies a dendritic resonance could easily be undetectable when using somatic input. Nevertheless, noise-driven membrane-potential oscillations caused by dendritic resonance can propagate to the soma where they can be recorded, hence contrasting with the low-pass filtering at the soma. We conclude that non-uniform distributions of active conductances can underlie differential filtering of synaptic input in neurons with spatially extended dendrites, like pyramidal neurons, bearing relevance for the localization-dependent targeting of synaptic input pathways to these cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Algorithms*
  • Animals
  • Brain / cytology
  • Brain / physiology*
  • Dendrites / physiology*
  • Humans
  • Membrane Potentials / physiology
  • Models, Neurological*
  • Pyramidal Cells / physiology*
  • Synapses / physiology
  • Synaptic Transmission / physiology

Grant support

This work was funded by the German Federal Ministry of Education and Research (01GQ0901, 01GQ1001A, 01GQ0972), Deutsche Forschungsgemeinschaft (SFB 618/B1 and GK1589), and the Einstein Foundation Berlin. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.