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Flight Motor Networks Modulate Primary Olfactory Processing in the Moth Manduca Sexta

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Flight Motor Networks Modulate Primary Olfactory Processing in the Moth Manduca Sexta Flight motor networks modulate primary olfactory processing in the moth Manduca sexta Phillip D. Chapmana,1, Rex Burklanda,1, Samual P. Bradleya, Benjamin Houota,2, Victoria Bullmana, Andrew M. Dacksa, and Kevin C. Dalya,3 aDepartment of Biology, West Virginia University, Morgantown, WV 26506 Edited by John G. Hildebrand, University of Arizona, Tucson, AZ, and approved April 11, 2018 (received for review December 23, 2017) Nervous systems must distinguish sensory signals derived from an signal analysis, or sensory motor learning (e.g., refs. 5 and 6) can animal’s own movements (reafference) from environmentally de- be classified as higher-order CDCs (2). Given their fundamental rived sources (exafference). To accomplish this, motor networks role in sensory-motor interactions, evidence of CDCs have been producing reafference transmit motor information, via a corollary observed in vision (2, 5–7), hearing (4, 8, 9), and the sensing of discharge circuit (CDC), to affected sensory networks, modulating body posture (10, 11), and their failure likely underlies sensory sensory function during behavior. While CDCs have been described hallucinations in schizophrenia (12), Parkinson’s disease (13), and in most sensory modalities, none have been observed projecting to dyspnea (14). Indeed, CDCs have been characterized to some an olfactory pathway. In moths, two mesothoracic to deutocerebral degree in nearly every sensory domain except olfaction, and to histaminergic neurons (MDHns) project from flight sensorimotor date no higher-order CDC has been described in any invertebrate centers in the mesothoracic neuromere to the antennal lobe (AL), nervous system. where they provide the sole source of histamine (HA), but whether Like eye saccades in vertebrates, active olfactory sampling they represent a CDC is unknown. We demonstrate that MDHn behaviors, such as sniffing, antennal and tongue flicking, and spiking activity is positively correlated with wing-motor output wing beating are periodic (15). These active sampling behaviors and increased before bouts of motor activity, suggesting that increase airflow and turbulence around the olfactory epithelium, MDHns communicate global locomotor state, rather than providing inducing a mechanosensory component to olfactory neural re- a precisely timed motor copy. Within the AL, HA application sharp- sponses observable even in the absence of odor (16–19). In the Manduca sexta NEUROSCIENCE ened entrainment of projection neuron responses to odor stimuli hawkmoth and other related insects, wing beat- – ing, in addition to casting back and forth through odor plumes, is embedded within simulated wing-beat induced flows, whereas – MDHn axotomy or AL HA receptor (HA-r) blockade reduced entrain- an important component of active odor-sampling behavior (20 ment. This finding is consistent with higher-order CDCs, as the 22). Wing beating can generate substantial oscillatory airflow MDHns enhanced rather than filtered entrainment of AL projection over the antennae (23) and vibrates the antennae at the fre- quency of the beating wing during flight (24). This implies that neurons. Finally, HA-r blockade increased odor detection and dis- during odor-guided flight, olfactory sensory neurons on the an- crimination thresholds in behavior assays. These results establish tennae are periodically exposed to odorant molecules in higher 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 Significance highlights the importance of motor-to-sensory signaling as a context-specific mechanism that fine-tunes sensory function. Across vertebrates and invertebrates, corollary discharge circuits (CDCs) project to and inform sensory networks about an ani- corollary discharge | olfaction | antennal lobe | active sampling | mal’s movements, which directly impact sensory processing. ascending neuron Failure of CDCs likely underlie sensory hallucinations in schizo- phrenia, Parkinson’s disease, and dyspnea, highlighting the fundamental importance of CDCs for successfully interpreting s animals locomote, their motor actions can directly affect sensory cues to adaptively interact with the external world. sensory function, causing self-induced, or “reafferent,” sensory A Ultimately, understanding the role of CDCs in integrating neural responses. Unchecked, reafference can interfere with sensory motor function will be vital to understand these dis- or otherwise influence the experience of externally derived or eases, but mechanistically little is known about how CDCs “exafferent” sensory cues. Furthermore, behaviors causing reaf- function. CDCs have been identified in most sensory domains ference can be an integral component of active sensory sampling except olfaction. Our findings indicate that a histaminergic CDC strategies. For example, saccadic eye movements continually enhances the ability of the olfactory system to more precisely shift the retinal image in a ballistic fashion to interrogate the encode stimulus temporal structure, resulting in enhanced visual environment and yet visual experience is perceived as olfactory acuity. stable. This visual stabilization likely occurs because the superior colliculus sends information about eye-movement commands Author contributions: P.D.C., R.B., B.H., A.M.D., and K.C.D. designed research; P.D.C., R.B., to the frontal eye field of the cortex (1). Such motor-to-sensory S.P.B., B.H., and V.B. performed research; P.D.C., R.B., S.P.B., B.H., V.B., and K.C.D. ana- pathways are referred to as corollary discharge circuits (CDCs), lyzed data; and P.D.C., R.B., and K.C.D. wrote the paper. which are a class of forward circuits that specifically provide in- The authors declare no conflict of interest. formation about motor activity to sensory systems, allowing them This article is a PNAS Direct Submission. to account for behavior-induced effects on sensory function. This open access article is distributed under Creative Commons Attribution-NonCommercial- CDCs can provide precisely timed facsimiles of motor commands NoDerivatives License 4.0 (CC BY-NC-ND). (i.e., an efference copy) to modulatory-like signals that represent 1P.D.C. and R.B. contributed equally to this work. current or pending changes in behavioral state (2). While all 2Present address: Division of Chemical Ecology, Department of Plant Protection Biology, CDCs provide motor information to sensory systems, they can be Swedish University of Agricultural Sciences, S-230 53 Alnarp, Sweden. further classified based on their functional consequences on sen- 3To whom correspondence should be addressed. Email: [email protected]. sory processing. CDCs that filter out reafferent inputs or inhibit This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. sensory-driven reflexes (e.g., refs. 3 and 4) are classified as lower- 1073/pnas.1722379115/-/DCSupplemental. order CDCs, while those that predict, stabilize, facilitate sensory www.pnas.org/cgi/doi/10.1073/pnas.1722379115 PNAS Latest Articles | 1of6 Downloaded by guest on September 25, 2021 velocity flows induced by wing beating, presumably enhancing house flight central pattern-generating circuitry, including wing odor–receptor interactions (21). Far from hindering moths, peri- sensory input (36–38). To characterize the relationship between odic odor stimulation is readily tracked by both local interneurons the MDHns and wing-motor output, we developed an approach (LNs) and projection neurons (PNs) of the antennal lobe (AL; the that leaves the entire central nervous system intact, exposing primary olfactory network) up to but not beyond ∼28 Hz, the the mesothoracic neuromere where all sensory motor nerves maximum wing-beat frequency of this species (25). Pulsed delivery emanating from the thoracic neuromeres were sectioned for of odors elicits more distinctive AL odor representations relative stability; this also allowed us to make intracellular recordings to continuous odor stimulation (18), and appears to be required from individual MDHns while simultaneously recording fore- for several moth species to track and locate odor sources (20, 26, wing depressor and elevator motor neuron output from the 27). In theory, the ability to track odors presented in the wing-beat trunk IIN1b fiber using a suction electrode (39) (Fig. 1A). In- frequency range could arise from purely feedforward mechanisms tracellular electrode guidance to MDHns was visually blind, but (28). However, AL neural tracking of stimuli presented across the spike shape and a tonic firing pattern guided selection of spe- wing-beat frequency range (0–28 Hz) requires neural connectivity cific cells for recording. Each recorded cell was dye-filled, and between flight motor circuits in the thoracic neuromeres and the HA-immunolabeling was used to confirm that an MDHn was AL (25), suggesting that motor centers may directly influence the recorded (Fig. 1B). temporal resolution of the olfactory system. The only known All recorded MDHns (n = 5) produced highly stereotyped connection between the flight-motor pattern-generating centers spike waveforms and were tonically active even in the absence of and the olfactory system in M. sexta is a single pair of mesothoracic motor output (Fig. 1C). In four of the five animals we were able to deutocerebral histaminergic (HA) neurons (MDHns); these to the hold intracellular recording long enough to induce wing- − cells represent
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