Oscillations of the Transepithelial Potential of Moth Olfactory Sensilla Are Influenced by Octopamine and Serotonin

Abstract

SUMMARY The biogenic amine octopamine is known to enhance the sensitivity of male moths to their species-specific pheromones in flight-tunnel experiments. This sensitization of pheromone-guided upwind flight is at least partly due to octopamine-dependent increases in the peak nerve impulse frequency of the pheromone response of olfactory receptor neurons. It is not known, however,whether octopamine exerts its effects directly on the electrical properties of the olfactory receptor neurons or indirectly, via modulation of the accessory cells of the sensillum. In extracellular tip recordings of pheromone-dependent trichoid sensilla on the antennae of male Manduca sexta moths, we investigated the effects of octopamine and serotonin on the transepithelial potential, which is generated by the activity of V-ATPases in sensillar accessory cells. In addition, the action potential activity of unstimulated olfactory receptor neurons was examined in the presence of biogenic amines. Under constant environmental conditions, the transepithelial potential oscillated regularly with periods of 2-8 min and with a 1-25 mV peak-to-peak amplitude over periods of several hours. These oscillatory intervals were interrupted by periods of relatively stable transepithelial potential, correlated with flight activity by the moth. Octopamine reduced the amplitude of the transepithelial potential oscillation and decreased the resistance of the sensillum preparation in a dose-dependent manner. Serotonin altered the waveform of the transepithelial potential, but did not change the resistance of the preparation. Thus, both amines affect the accessory cells, but have different targets in the regulation of the transepithelial potential. Neither amine significantly influenced the spontaneous action potential activity of the olfactory receptor neurons.

Serotonin/GABA receptors modulate odor input to olfactory receptor neuron in locusts

“…By measuring the responses of ORNs after suppressing the expression of corresponding genes, we demonstrated that the Lmig5-HT 2 receptor plays an inhibitory role in the response of ORNs to odorants, which results in the regulation of the signal output. Previous studies in moths suggested that 5-HT 2 in the sensillum, lymph might regulate neuronal activity by altering the transepithelial potential, thus changing the threshold of firing without influencing the spontaneous action potential activity of ORNs (Dolzer et al, 2001). Because ORNs performed in very similar patterns when locusts had knockdown of GABA b , we suggest that regulation by the Lmig5-HT 2 receptor may indirectly Our findings indicate that the depression of the 5-HT 2 and GABA b receptors increased sensory responses to odors, and in other words, the 5-HT 2 and GABA b attenuated sensory response.…”

“…The odorants pass through the pores on the sensillar wall and are then bound by OBPs that are secreted by accessory cells to form the odorant/OBP complex, which is transported onto ORs and OR co-receptors on the membranes of ORN dendrites, thus evoking action potentials in ORNs (Laughlin et al, 2008). Studies have shown that in the antennae of male Manduca sexta moths, 5-HT affects the transepithelial potential, generated by accessory cells in the olfactory sensillum and creates a driving force for the receptor current (Dolzer et al, 2001;Grosmaitre et al, 2001), whereas it has no direct effect on the activity of spontaneous action potential of olfactory receptor neurons (Dolzer et al, 2001). This is consistent with our results that the 5-HT receptor is expressed in the accessory cells but not on ORNs, which suggests that 5-HT acts directly on accessory cells to affect the ORNs when acting in the peripheral nervous system, rather than directly on ORNs.…”

“…Moreover, 5-HT enhances the response of inhibitory local interneurons, GABAergic neurons, which indirectly results in reduced neurotransmitter release from ORN terminals via GABA b receptor-dependent presynaptic inhibition (Dacks et al, 2009;Dugué and Mainen, 2009;Petzold et al, 2009). Nevertheless, very few studies have focused on the role of 5-HT at the peripheral level (Dolzer et al, 2001). 5-HT is found in the hemolymph of insects (Lange et al, 1989;Siju et al, 2008;Zhukovskaya and Polyanovsky, 2017).…”

Neuromuscular Anatomy and Motor Patterns at the Base of Calling Behaviour in the Female Spongy Moth Lymantria dispar

“…The spontaneous spike activity recorded from each of the TAG nerves N4 to N6 was analysed by means of the Clampfit 10.0 software (Axon Instruments) [ 42 , 43 , 44 ]. Spikes in the discharges were sorted out by a threshold-based search and then their peak-to-peak amplitude (PPA) and the max decay slope (MDS) of each spike were measured as an index of their amplitude and shape, respectively, and plotted versus the time of occurrence.…”

Contribution of membrane-associated oscillators to biological timing at different timescales

“…An example of non-associative learning is adaptation of olfactory sensory neurons. Olfactory adaptation employs, e.g., Ca 2+ -dependent negative feedback control mechanisms to prevent damage via overstimulation after a very strong or long odor/pheromone stimulus ( Zufall and Leinders-Zufall, 2000 ; Dolzer et al, 2001 ; Spehr et al, 2009 ; Stengl, 2010 ). Hebbian plasticity mechanisms shift the current physiological dynamic setpoint to a new dynamic setpoint, for example, measurable as shifted dose-response curve of the sensory neurons.…”