Functional organization of male-specific olfactory glomeruli in the sphinx moth Manduca sexta

Abstract

The macroglomerular complex (MGC) in the antennal lobe of the sphinx moth Manduca sexta is the first brain region for processing sex-pheromonal information. How is the MGC is functionally organized, and how are chemical and physical features of the pheromone encoded by projection neurons (PNs) innervating the MGC (MGC-PNs). For some MGC-PNs with arborizations in the toroid, one of the two major glomeruli of the MGC, bombykal (a key pheromone component) can evoke a mixed (inhibitory/excitatory/inhibitory) response similar to that evoked by the pheromone blend. Likewise, for some neurons with arborizations in the cumulus, C-15 (a mimic of the second key component) can evoke a similar mixed response. The maximal pulse frequency encoded by these component-specific neurons was not increased in the presence of the blend, but seemed to arise through the convergence of two parallel pathways, one excitatory and one inhibitory, both activated by the same olfactory stimulus. Convergence of different synaptic pathways allowed MGC-PNs to resolve intermittent stimuli and thus to relay the temporal structure of the pheromonal signal to higher brain centers. In a subset of MGC-PNs that was excited by antennal stimulation with either of the two components (bombykal-C-15 cells, blend neurons), the ability to encode intermittent stimuli was improved when stimulating with the blend. The temporal character of the responses was dependent on the ratio of the two key components in the blend. Component-specific MGC-PNs responded over a range of increasing pheromone concentration with stronger inhibitory and excitatory postsynaptic potentials and more impulses but the responses were not affected by changing the blend ratio. Two basic response patterns emerged when the ipsilateral antennal flagellum was stimulated at different zones along its proximo-distal axis while the activity of MGC-PNs was recorded. A subset of neurons with broad receptive fields was excited regardless of the zone of the antenna stimulated, whereas another subset responded selectively to stimulation of the basal region of the antenna. A diverse array of MGC-PNs forms a heterogeneous group of parallel output channels that encode features of the pheromone signal that the moth is likely to encounter in the natural stimulus situation.