Animals use behaviors to actively sample the environment across a broad spectrum of sensory domains. These behaviors discretize the sensory experience into unique spatiotemporal moments, minimize sensory adaptation, and enhance perception. In olfaction, behaviors such as sniffing, antennal flicking, and wing beating all act to periodically expose olfactory epithelium. In mammals, it is thought that sniffing enhances neural representations; however, the effects of insect wing beating on representations remain unknown. To determine how well the antennal lobe (AL) produces odor dependent representations when wing beating effects are simulated, we used extracellular methods to record neural units and local field potentials (LFPs) from moth AL. We recorded responses to odors presented as prolonged continuous stimuli or periodically as 20 and 25 Hz pulse trains designed to simulate the oscillating effects of wing beating around the antennae during odor guided flight. Using spectral analyses, we show that ~25% of all recorded units were able to entrain to “pulsed stimuli”; this includes pulsed blanks, which elicited the strongest overall entrainment. The strength of entrainment to pulse train stimuli was dependent on molecular features of the odorants, odor concentration, and pulse train duration. Moreover, units showing pulse tracking responses were highly phase locked to LFPs during odor stimulation, indicating that unit-LFP phase relationships are stimulus-driven. Finally, a Euclidean distance-based population vector analysis established that AL odor representations are more robust, peak more quickly, and do not show adaptation when odors were presented at the natural wing beat frequency as opposed to prolonged continuous stimulation. These results suggest a general strategy for optimizing olfactory representations, which exploits the natural rhythmicity of wing beating by integrating mechanosensory and olfactory cues at the level of the AL.

SignificanceAcross vertebrates and invertebrates, corollary discharge circuits (CDCs) project to and inform sensory networks about an animal’s movements, which directly impact sensory processing. Failure of CDCs likely underlie sensory hallucinations in schizophrenia, Parkinson’s disease, and dyspnea, highlighting the fundamental importance of CDCs for successfully interpreting sensory cues to adaptively interact with the external world. Ultimately, understanding the role of CDCs in integrating sensory motor function will be vital to understand these diseases, but mechanistically little is known about how CDCs function. CDCs have been identified in most sensory domains except olfaction. Our findings indicate that a histaminergic CDC enhances the ability of the olfactory system to more precisely encode stimulus temporal structure, resulting in enhanced olfactory acuity.

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Animals that plume track have developed navigational strategies that optimize the ability to track an odor to its source. This movement is an active part of the olfactory experience. For vertebrates, sniffing is also an active part of the olfactory experience that controls the speed and regularity of odor interactions with the olfactory receptors. This sniffing is coincident with locomotion throughout the environment and head movement back and forth across an odor plume. Similarly, moths actively beat their wings as they encounter odor plumes. In Manduca sexta, this wing beating influences speed and regularity of olfactory input in such a way that odor processing and perception are enhanced. While it is clear that the antennal lobe (AL) of M. sexta has evolved to process these naturally encountered olfactory stimuli, there may be a source of input that optimizes processing only when odor is sampled through wing beating. In other sensory systems, corollary discharge (CD) mechanisms have evolved to enhance sensory processing when the sensory input is caused by an animal's own muscle movement, termed reafference. These CD circuits exhibit a functional neural connection, either direct or indirect, between the sensory system and the motor system that caused the reafference. In M. sexta, there is a candidate pair of histamine (HA) immunoreactive neurons that project from the mesothoracic ganglia to the ALs. The goal of this study was to functionally characterize the role of HA signaling within the AL of M. sexta using pharmacological injections and behavioral detection assays. Here we have shown that pharmacological disruption of normal histamine signaling within the AL reduces sensitivity. This provides the first functional characterization of an olfactory CD circuit that uses flight-motor information to mediate olfactory sensitivity.