The anatomical basis for modulatory convergence in the antennal lobe of Manduca sexta

J Comp Neurol. 2016 Jun 15;524(9):1859-75. doi: 10.1002/cne.23926. Epub 2015 Dec 29.

Abstract

The release of neuromodulators by widely projecting neurons often allows sensory systems to alter how they process information based on the physiological state of an animal. Neuromodulators alter network function by changing the biophysical properties of individual neurons and the synaptic efficacy with which individual neurons communicate. However, most, if not all, sensory networks receive multiple neuromodulatory inputs, and the mechanisms by which sensory networks integrate multiple modulatory inputs are not well understood. Here we characterized the relative glomerular distribution of two extrinsic neuromodulators associated with distinct physiological states, serotonin (5-HT) and dopamine (DA), in the antennal lobe (AL) of the moth Manduca sexta. By using immunocytochemistry and mass dye fills, we characterized the innervation patterns of both 5-HT- and tyrosine hydroxylase-immunoreactive processes relative to each other, to olfactory receptor neurons (ORNs), to projection neurons (PNs), and to several subsets of local interneurons (LNs). 5-HT immunoreactivity had nearly complete overlap with PNs and LNs, yet no overlap with ORNs, suggesting that 5-HT may modulate PNs and LNs directly but not ORNs. TH immunoreactivity overlapped with PNs, LNs, and ORNs, suggesting that dopamine has the potential to modulate all three cell types. Furthermore, the branching density of each neuromodulator differed, with 5-HT exhibiting denser arborizations and TH-ir processes being sparser. Our results suggest that 5-HT and DA extrinsic neurons target partially overlapping glomerular regions, yet DA extends further into the region occupied by ORNs.

Keywords: AB_2313880; AB_2313973; AB_2314803; AB_2314866; AB_2341129; dopamine; neuromodulation; olfaction, insect; serotonin.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arthropod Antennae / anatomy & histology*
  • Dextrans / metabolism
  • Dopamine / metabolism
  • Drosophila Proteins / metabolism
  • Insect Hormones / metabolism
  • Manduca / anatomy & histology*
  • Nerve Net / physiology*
  • Neuropeptides / metabolism
  • Neurotransmitter Agents / metabolism*
  • Olfactory Receptor Neurons / metabolism*
  • Serotonin / metabolism
  • Tachykinins

Substances

  • BRP protein, Drosophila
  • Dextrans
  • Drosophila Proteins
  • Insect Hormones
  • Neuropeptides
  • Neurotransmitter Agents
  • Tachykinins
  • allatostatin
  • Serotonin
  • allatotropin
  • Dopamine