Odor Detection in Manduca sexta Is Optimized when Odor Stimuli Are Pulsed at a Frequency Matching the Wing Beat during Flight

Abstract

Sensory systems sample the external world actively, within the context of self-motion induced disturbances. Mammals sample olfactory cues within the context of respiratory cycles and have adapted to process olfactory information within the time frame of a single sniff cycle. In plume tracking insects, it remains unknown whether olfactory processing is adapted to wing beating, which causes similar physical effects as sniffing. To explore this we first characterized the physical properties of our odor delivery system using hotwire anemometry and photo ionization detection, which confirmed that odor stimuli were temporally structured. Electroantennograms confirmed that pulse trains were tracked physiologically. Next, we quantified odor detection in moths in a series of psychophysical experiments to determine whether pulsing odor affected acuity. Moths were first conditioned to respond to a target odorant using Pavlovian olfactory conditioning. At 24 and 48 h after conditioning, moths were tested with a dilution series of the conditioned odor. On separate days odor was presented either continuously or as 20 Hz pulse trains to simulate wing beating effects. We varied pulse train duty cycle, olfactometer outflow velocity, pulsing method, and odor. Results of these studies, established that detection was enhanced when odors were pulsed. Higher velocity and briefer pulses also enhanced detection. Post hoc analysis indicated enhanced detection was the result of a significantly lower behavioral response to blank stimuli when presented as pulse trains. Since blank responses are a measure of false positive responses, this suggests that the olfactory system makes fewer errors (i.e. is more reliable) when odors are experienced as pulse trains. We therefore postulate that the olfactory system of Manduca sexta may have evolved mechanisms to enhance odor detection during flight, where the effects of wing beating represent the norm. This system may even exploit temporal structure in a manner similar to sniffing.

Co-option of a motor-to-sensory histaminergic circuit correlates with insect flight biomechanics

“…In addition, neural population responses from the AL of M. sexta track and represent olfactory stimuli optimally when odours are presented at the wing-beat frequency [23]. This finding also corresponds to enhanced olfactory acuity as measured behaviourally [55], supporting the conclusion that their olfactory system has adapted to encode information that is embedded within a temporal structure induced by their own active sampling behaviour. The disturbances caused by the very high frequency wing beating in D. melanogaster on the other hand, are unlikely to be tracked by the AL, although there is clear evidence that the mechanoacoustic signature of the wing beat is detected by the arista and processed in the AMMC [56,57].…”

Transmitter Co-Expression Reveals Key Organizational Principles of Local Interneuron Heterogeneity in the Olfactory System

“…Animals: Manduca sexta were raised at West Virginia University as previously described (Bell and Joachim, 1976;Daly et al, 2013). Equal numbers of males and females were pooled for all data.…”

The anatomical basis for modulatory convergence in the antennal lobe of Manduca sexta

“…Manduca sexta (hereafter referred to as Manduca ) were raised at West Virginia University on a 16:8‐hour reverse light:dark cycle in the laboratory of Dr. Kevin Daly as previously described (Bell and Joachim, ; Daly et al, ). Equal numbers of males and females were used, and a minimum of 6 moths were used for each protocol.…”