Dendritic Organization of Olfactory Inputs to Medial Amygdala Neurons

J Neurosci. 2015 Sep 23;35(38):13020-8. doi: 10.1523/JNEUROSCI.0627-15.2015.

Abstract

The medial amygdala (MeA) is a central hub in the olfactory neural network. It receives vomeronasal information directly from the accessory olfactory bulb (AOB) and main olfactory information largely via odor-processing regions such as the olfactory cortical amygdala (CoA). How these inputs are processed by MeA neurons is poorly understood. Using the GAD67-GFP mouse, we show that MeA principal neurons receive convergent AOB and CoA inputs. Somatically recorded AOB synaptic inputs had slower kinetics than CoA inputs, suggesting that they are electrotonically more distant. Field potential recording, pharmacological manipulation, and Ca(2+) imaging revealed that AOB synapses are confined to distal dendrites and segregated from the proximally located CoA synapses. Moreover, unsynchronized AOB inputs had significantly broader temporal summation that was dependent on the activation of NMDA receptors. These findings show that MeA principal neurons process main and accessory olfactory inputs differentially in distinct dendritic compartments. Significance statement: In most vertebrates, olfactory cues are processed by two largely segregated neural pathways, the main and accessory olfactory systems, which are specialized to detect odors and nonvolatile chemosignals, respectively. Information from these two pathways ultimately converges at higher brain regions, one of the major hubs being the medial amygdala. Little is known about how olfactory inputs are processed by medial amygdala neurons. This study shows that individual principal neurons in this region receive input from both pathways and that these synapses are spatially segregated on their dendritic tree. We provide evidence suggesting that this dendritic segregation leads to distinct input integration and impact on neuronal output; hence, dendritic mechanisms control olfactory processing in the amygdala.

Keywords: dendrite; emotion; mating; olfaction; reproduction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / genetics
  • Afferent Pathways / drug effects
  • Afferent Pathways / physiology*
  • Animals
  • Calcium / metabolism
  • Central Nervous System Stimulants / pharmacology
  • Corticomedial Nuclear Complex / cytology*
  • Dendrites / drug effects
  • Dendrites / physiology*
  • Excitatory Amino Acid Antagonists / pharmacology
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / genetics
  • Glutamate Decarboxylase / genetics
  • Glutamate Decarboxylase / metabolism
  • In Vitro Techniques
  • Mice
  • Mice, Transgenic
  • Neurons / cytology*
  • Neurons / physiology
  • Olfactory Bulb / physiology*
  • Patch-Clamp Techniques
  • Picrotoxin / pharmacology
  • Quinoxalines / pharmacology
  • Sodium Channel Blockers / pharmacology
  • Tetrodotoxin / pharmacology
  • Valine / analogs & derivatives
  • Valine / pharmacology

Substances

  • Central Nervous System Stimulants
  • Excitatory Amino Acid Antagonists
  • Quinoxalines
  • Sodium Channel Blockers
  • 2,3-dioxo-6-nitro-7-sulfamoylbenzo(f)quinoxaline
  • Picrotoxin
  • Tetrodotoxin
  • 2-amino-5-phosphopentanoic acid
  • Glutamate Decarboxylase
  • glutamate decarboxylase 1
  • Valine
  • Calcium