Biophysical constraints on lateral inhibition in the olfactory bulb

J Neurophysiol. 2016 Jun 1;115(6):2937-49. doi: 10.1152/jn.00671.2015. Epub 2016 Mar 23.

Abstract

The mitral cells (MCs) of the mammalian olfactory bulb (OB) constitute one of two populations of principal neurons (along with middle/deep tufted cells) that integrate afferent olfactory information with top-down inputs and intrinsic learning and deliver output to downstream olfactory areas. MC activity is regulated in part by inhibition from granule cells, which form reciprocal synapses with MCs along the extents of their lateral dendrites. However, with MC lateral dendrites reaching over 1.5 mm in length in rats, the roles of distal inhibitory synapses pose a quandary. Here, we systematically vary the properties of a MC model to assess the capacity of inhibitory synaptic inputs on lateral dendrites to influence afferent information flow through MCs. Simulations using passivized models with varying dendritic morphologies and synaptic properties demonstrated that, even with unrealistically favorable parameters, passive propagation fails to convey effective inhibitory signals to the soma from distal sources. Additional simulations using an active model exhibiting action potentials, subthreshold oscillations, and a dendritic morphology closely matched to experimental values further confirmed that distal synaptic inputs along the lateral dendrite could not exert physiologically relevant effects on MC spike timing at the soma. Larger synaptic conductances representative of multiple simultaneous inputs were not sufficient to compensate for the decline in signal with distance. Reciprocal synapses on distal MC lateral dendrites may instead serve to maintain a common fast oscillatory clock across the OB by delaying spike propagation within the lateral dendrites themselves.

Keywords: cable theory; computational neuroscience; lateral dendrites; mitral cell; olfaction.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cell Shape / physiology
  • Cell Size
  • Computer Simulation
  • Electric Impedance
  • Membrane Potentials / physiology
  • Models, Neurological
  • Neural Inhibition / physiology*
  • Neurons / cytology
  • Neurons / physiology*
  • Olfactory Bulb / cytology
  • Olfactory Bulb / physiology*
  • Receptors, GABA-A / metabolism
  • Smell / physiology
  • Synapses / physiology*

Substances

  • Receptors, GABA-A