Transplant Antennae and Host Brain Interact to Shape Odor Perceptual Space in Male Moths

PLoS One. 2016 Jan 27;11(1):e0147906. doi: 10.1371/journal.pone.0147906. eCollection 2016.

Abstract

Behavioral responses to odors rely first upon their accurate detection by peripheral sensory organs followed by subsequent processing within the brain's olfactory system and higher centers. These processes allow the animal to form a unified impression of the odor environment and recognize combinations of odorants as single entities. To investigate how interactions between peripheral and central olfactory pathways shape odor perception, we transplanted antennal imaginal discs between larval males of two species of moth Heliothis virescens and Heliothis subflexa that utilize distinct pheromone blends. During metamorphic development olfactory receptor neurons originating from transplanted discs formed connections with host brain neurons within olfactory glomeruli of the adult antennal lobe. The normal antennal receptor repertoire exhibited by males of each species reflects the differences in the pheromone blends that these species employ. Behavioral assays of adult transplant males revealed high response levels to two odor blends that were dissimilar from those that attract normal males of either species. Neurophysiological analyses of peripheral receptor neurons and central olfactory neurons revealed that these behavioral responses were a result of: 1. the specificity of H. virescens donor olfactory receptor neurons for odorants unique to the donor pheromone blend and, 2. central odor recognition by the H. subflexa host brain, which typically requires peripheral receptor input across 3 distinct odor channels in order to elicit behavioral responses.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Arthropod Antennae / physiology*
  • Behavior, Animal
  • Brain / cytology
  • Brain / physiology
  • Male
  • Moths / physiology*
  • Odorants / analysis
  • Olfactory Pathways*
  • Olfactory Perception*
  • Olfactory Receptor Neurons / metabolism
  • Pheromones / metabolism*
  • Smell

Substances

  • Pheromones

Grants and funding

National Science Foundation 0640655 (CEL), National Science Foundation 0641014 (NJV), and National Science Foundation 1147233 (NJV) (www.nsf.gov). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.