Abstract

Neural circuits projecting information from motor to sensory pathways are common across sensory domains. These circuits typically modify sensory function as a result of motor pattern activation; this is particularly so in cases where the resultant behavior affects the sensory experience or its processing. However, such circuits have not been observed projecting to an olfactory pathway in any species despite well characterized active sampling behaviors that produce reafferent mechanical stimuli, such as sniffing in mammals and wing beating in the moth Manduca sexta. In this study we characterize a circuit that connects a flight sensory-motor center to an olfactory center in Manduca. This circuit consists of a single pair of histamine immunoreactive (HA-ir) neurons that project from the mesothoracic ganglion to innervate a subset of ventral antennal lobe (AL) glomeruli. Furthermore, within the AL we show that the M. sexta histamine B receptor (MsHisClB) is exclusively expressed by a subset of GABAergic and peptidergic LNs, which broadly project to all olfactory glomeruli. Finally, the HA-ir cell pair is present in fifth stage instar larvae; however, the absence of MsHisClB-ir in the larval antennal center indicates that the circuit is incomplete prior to metamorphosis and importantly prior to the expression of flight behavior. Although the functional consequences of this circuit remain unknown, these results provide the first detailed description of a circuit that interconnects an olfactory system with motor centers driving flight behaviors including odor-guided flight.

Highlights

  • Animals exhibit stereotypical search behaviors in pursuit of potential food sources or mating partners

  • Motor-to-sensory circuits have been extensively characterized in many sensory systems, there is a dearth of detailed descriptions of input from motor to olfactory centers

  • Nervous systems have concurrently evolved circuits that provide information to sensory systems about impending behaviors that will affect sensory input. This has been well-documented in many sensory systems, very little is known about neural circuits projecting from neural centers governing odor-guided behaviors to olfactory networks

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Summary

Introduction

Animals exhibit stereotypical search behaviors in pursuit of potential food sources or mating partners. Some animals employ sampling strategies where rhythmic motor patterns optimize the interaction between stimuli and their affected sensory systems. Many of these motor systems project to and modulate how sensory systems process this information. Flight Motor to Olfactory Circuit these small movements send a signal canceling the perception of a moving scene, affording proper behavioral responses to other stimuli in the environment (Zaretsky and Rowell, 1979; Ross et al, 2001). Other motor to sensory circuits have been shown to amplify self-induced communication signals (Mohr et al, 2003), inhibit reflex responses (Chalfie et al, 1985), and are involved in sensory/motor planning (Brainard and Doupe, 2000; Sommer and Wurtz, 2002). While work in other sensory systems have made significant progress in characterizing motor to sensory circuits (Crapse and Sommer, 2008), it is not clear whether such circuits are present in the olfactory system

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