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.
Highlights
The insect olfactory system is comprised of a peripheral structure that interacts with the fluid environment and captures odorous molecules that are presented to receptor sites on olfactory receptor neurons [1]
The behavioral responses of moths often rely upon the presence of a blend of odorants and, as such, a function of higher olfactory pathways and processing in the brain must be to interpret the activity across olfactory glomeruli and construct a unified impression of the complete odor that interacted with receptors at the periphery
The remaining 188 transplant males (54%) exhibited the first in a sequence of orientation behaviors beginning with upwind oriented flight in the odor plume (UP), followed by flight to midway (MID) and source contact (SC) in response to at least one of four odor sources (Fig 2)
Summary
The insect olfactory system is comprised of a peripheral structure that interacts with the fluid environment and captures odorous molecules that are presented to receptor sites on olfactory receptor neurons [1]. Simultaneous activation of three separate olfactory pathways, tuned to Z11-16:Ald, (Z)-9-hexadecenal (Z9-16: Ald), and (Z)-11-hexadecenol (Z11-16:OH) respectively, is crucial to elicit attractive behavior in male H. subflexa, [12,13,14] These differences are reflected in the odor sensitivity profiles of peripheral receptor neurons located on the antennae of each species [14]. Vickers et al [22,23] extended this technique by transplanting antennal imaginal discs across two related species (H. virescens and another Heliothine moth, Helicoverpa zea) The results of these various studies indicated that the donor antenna dictates the glomerular arrangement of the antennal lobe some individuals with aglomerular or disorganized antennal lobe structure were still capable of odor-mediated flight [18,22,23,24]. The behavioral requirements for different blends reflect the olfactory receptor repertoire characteristic of the normal donor antenna and central constraints imposed by connections in the host brain
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