Efficient Low-Pass Dendro-Somatic Coupling in the Apical Dendrite of Layer 5 Pyramidal Neurons in the Anterior Cingulate Cortex

J Neurosci. 2020 Nov 11;40(46):8799-8815. doi: 10.1523/JNEUROSCI.3028-19.2020. Epub 2020 Oct 12.

Abstract

Signal propagation in the dendrites of many neurons, including cortical pyramidal neurons in sensory cortex, is characterized by strong attenuation toward the soma. In contrast, using dual whole-cell recordings from the apical dendrite and soma of layer 5 (L5) pyramidal neurons in the anterior cingulate cortex (ACC) of adult male mice we found good coupling, particularly of slow subthreshold potentials like NMDA spikes or trains of EPSPs from dendrite to soma. Only the fastest EPSPs in the ACC were reduced to a similar degree as in primary somatosensory cortex, revealing differential low-pass filtering capabilities. Furthermore, L5 pyramidal neurons in the ACC did not exhibit dendritic Ca2+ spikes as prominently found in the apical dendrite of S1 (somatosensory cortex) pyramidal neurons. Fitting the experimental data to a NEURON model revealed that the specific distribution of Ileak, Iir, Im , and Ih was sufficient to explain the electrotonic dendritic structure causing a leaky distal dendritic compartment with correspondingly low input resistance and a compact perisomatic region, resulting in a decoupling of distal tuft branches from each other while at the same time efficiently connecting them to the soma. Our results give a biophysically plausible explanation of how a class of prefrontal cortical pyramidal neurons achieve efficient integration of subthreshold distal synaptic inputs compared with the same cell type in sensory cortices.SIGNIFICANCE STATEMENT Understanding cortical computation requires the understanding of its fundamental computational subunits. Layer 5 pyramidal neurons are the main output neurons of the cortex, integrating synaptic inputs across different cortical layers. Their elaborate dendritic tree receives, propagates, and transforms synaptic inputs into action potential output. We found good coupling of slow subthreshold potentials like NMDA spikes or trains of EPSPs from the distal apical dendrite to the soma in pyramidal neurons in the ACC, which was significantly better compared with S1. This suggests that frontal pyramidal neurons use a different integration scheme compared with the same cell type in somatosensory cortex, which has important implications for our understanding of information processing across different parts of the neocortex.

Keywords: NMDA spike; anterior cingulate cortex; biophysical model; dendrite; electrical properties; pyramidal neuron.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Animals
  • Dendrites / physiology*
  • Electrophysiological Phenomena
  • Excitatory Postsynaptic Potentials
  • Gyrus Cinguli / physiology*
  • In Vitro Techniques
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Optogenetics
  • Pyramidal Cells / physiology*
  • Receptors, N-Methyl-D-Aspartate / physiology
  • Somatosensory Cortex / physiology*

Substances

  • Receptors, N-Methyl-D-Aspartate