The influence of single bursts versus single spikes at excitatory dendrodendritic synapses

Eur J Neurosci. 2012 Feb;35(3):389-401. doi: 10.1111/j.1460-9568.2011.07978.x. Epub 2012 Jan 25.

Abstract

The synchronization of neuronal activity is thought to enhance information processing. There is much evidence supporting rhythmically bursting external tufted cells (ETCs) of the rodent olfactory bulb glomeruli coordinating the activation of glomerular interneurons and mitral cells via dendrodendritic excitation. However, as bursting has variable significance at axodendritic cortical synapses, it is not clear if ETC bursting imparts a specific functional advantage over the preliminary spike in dendrodendritic synaptic networks. To answer this question, we investigated the influence of single ETC bursts and spikes with the in vitro rat olfactory bulb preparation at different levels of processing, via calcium imaging of presynaptic ETC dendrites, dual electrical recording of ETC -interneuron synaptic pairs, and multicellular calcium imaging of ETC-induced population activity. Our findings supported single ETC bursts, versus single spikes, driving robust presynaptic calcium signaling, which in turn was associated with profound extension of the initial monosynaptic spike-driven dendrodendritic excitatory postsynaptic potential. This extension could be driven by either the spike-dependent or spike-independent components of the burst. At the population level, burst-induced excitation was more widespread and reliable compared with single spikes. This further supports the ETC network, in part due to a functional advantage of bursting at excitatory dendrodendritic synapses, coordinating synchronous activity at behaviorally relevant frequencies related to odor processing in vivo.

Publication types

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

MeSH terms

  • Action Potentials / physiology*
  • Animals
  • Calcium / metabolism
  • Calcium Signaling / physiology
  • Dendrites / physiology*
  • Excitatory Postsynaptic Potentials / physiology
  • Glutamic Acid / metabolism
  • Interneurons / physiology
  • Olfactory Bulb / cytology
  • Olfactory Bulb / physiology
  • Patch-Clamp Techniques
  • Rats
  • Rats, Sprague-Dawley
  • Sensory Receptor Cells / cytology
  • Sensory Receptor Cells / physiology
  • Synapses / physiology*
  • Synaptic Transmission / physiology*

Substances

  • Glutamic Acid
  • Calcium