Flight motor networks modulate primary olfactory processing in the moth Manduca sexta.

Nervous systems must distinguish sensory signals derived from an animal's own movements (reafference) from environmentally derived sources (exafference). To accomplish this, motor networks producing reafference transmit motor information, via a corollary discharge circuit (CDC), to affected sensory networks, modulating sensory function during behavior. While CDCs have been described in most sensory modalities, none have been observed projecting to an olfactory pathway. In moths, two mesothoracic to deutocerebral histaminergic neurons (MDHns) project from flight sensorimotor centers in the mesothoracic neuromere to the antennal lobe (AL), where they provide the sole source of histamine (HA), but whether they represent a CDC is unknown. We demonstrate that MDHn spiking activity is positively correlated with wing-motor output and increased before bouts of motor activity, suggesting that MDHns communicate global locomotor state, rather than providing a precisely timed motor copy. Within the AL, HA application sharpened entrainment of projection neuron responses to odor stimuli embedded within simulated wing-beat-induced flows, whereas MDHn axotomy or AL HA receptor (HA-r) blockade reduced entrainment. This finding is consistent with higher-order CDCs, as the MDHns enhanced rather than filtered entrainment of AL projection neurons. Finally, HA-r blockade increased odor detection and discrimination thresholds in behavior assays. These results establish MDHns as a CDC that modulates AL temporal resolution, enhancing odor-guided behavior. MDHns thus appear to represent a higher-order CDC to an insect olfactory pathway; this CDC's unique nature highlights the importance of motor-to-sensory signaling as a context-specific mechanism that fine-tunes sensory function.

Antennal lobe representations are optimized when olfactory stimuli are periodically structured to simulate natural wing beat effects.

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.