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

Significance

Across 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.

Abstract

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.