Male-specific, sex pheromone-selective projection neurons in the antennal lobes of the mothManduca sexta

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Abstract
A subset of olfactory projection neurons in the brain of maleManduca sexta is described, and their role in sex pheromone information processing is examined. These neurons have extensive arborizations in the macroglomerular complex (MGC), a distinctive and sexually dimorphic area of neuropil in the antennal lobe (AL), to which the axons of two known classes of antennal pheromone receptors project. Each projection neuron sends an axon from the AL into the protocerebrum (Figs. 4, 7, 9, 13 and 15). Forty-one projection neurons were characterized according to their responses to electrical stimulation of the antennal nerve as well as olfactory stimulation of antennal receptors (Fig. 1). All neurons exhibited strong selectivity for female sex pheromones. Other behaviorally relevant odors, such as plant volatiles, had no obvious effect on the activity of these neurons (Fig. 2). Two broad physiological categories were found: (a) cells that were excited by stimulation of the ipsilateral antenna with pheromones (29 out of 41), and (b) cells that received a mixed input (inhibition and excitation) from pheromone pathways (12 out of 41). Of the cells in the first category, 13 out of 29 were equally excited in response to stimulation of the antenna with either the principal natural pheromone (bombykal) or a mimic of a second unidentified pheromone (‘C-15’) and were similarly excited by the natural pheromone blend (Fig. 3). The remaining 16 out of 29 cells responded selectively, and in some cases, in a dose-dependent manner, to stimulation of the antenna with bombykal or C-15, but not both (Figs. 5, 6 and 8). Some of these neurons had dendritic arborizations restricted to only a portion of the MGC neuropil (Fig. 9), whereas most had arborizations throughout the MGC. Of the cells in the second category, 9 out of 12 were excited by bombykal, inhibited by C-l 5, and showed a mixed response to the natural pheromone blend (Figs. 11 and 12). For the other 3 out of 12 cells, the response polarity was reversed for the two chemically-identified odors (Fig. 14). Two additional neurons, which were not tested with olfactory stimuli, were tonically inhibited in response to electrical stimulation of the ipsilateral antennal nerve (Fig. 15). These observations suggest that some of the male-specific projection neurons may signal general pheromone-triggered arousal, whereas a smaller number can actively integrate inputs from the two known receptor classes (Bal- and C-15-selective) and may operate as ‘mixture detectors’ at this level of the olfactory subsystem that processes information about sex pheromones.