Serotonergic Modulation of Olfactory Processing in the Antennal Lobe of the Tobacco Hawkmoth, Manduca sexta

Abstract

The nervous system copes with variability in the external and internal environment by using neuromodulators to adjust the efficacy of neural circuits. The role of serotonin (5HT) as a neuromodulator of olfactory processing in the antennal lobe (AL) of Manduca sexta was examined. Serotonin has been hypothesized as a circadian modulator of sensitivity of AL neurons, so the coding of odor concentration in the AL was first examined without the manipulation of 5HT levels. Reponses of the AL to different concentrations of odors were recorded using multi-electrode extracellular arrays. As odor concentration increased, more AL units responded and the AL was best able to discriminate odors at high concentrations, a finding that was replicated in matched behavioral assays. Multi-electrode recordings were then used to examine the effects of 5HT on responses to stimuli that varied in chemical structure and concentration. Serotonin enhanced AL unit responses by increasing response duration and firing rate, which in turn increased the amount of coincident firing between units. Due to the increased activation of units as concentration increased, and the greater effect of 5HT on stronger responses, serotonin had the greatest effect on overall ensemble activation at higher odor concentrations. Additionally, response thresholds shifted to lower odor concentrations for some units, suggesting that 5HT increases the sensitivity of AL units. Serotonin enhanced AL discrimination of single odors at different concentrations and structurally dissimilar odors at a single concentration. In order to predict which insects share a similar role for 5HT in the AL, immunocytochemistry was used to compare the ALs of different insects. All holometabolous insects (except the Euhymenoptera) had 5HT-immunoreactive AL neurons that were morphologically similar to those of M. sexta. These combined studies implicate 5HT as a modulator of sensitivity and efficacy in the AL of M. sexta and suggest that 5HT may play this role for most of the Holometabola. This proposed role of 5HT in the AL of the Holometabola is reminiscent of the hypothesized involvement of serotonergic neurons from the Raphe nucleus in vertebrates that seem to gate activity in the olfactory bulb in the context of behavioral arousal.