Co-option of a motor-to-sensory histaminergic circuit correlates with insect flight biomechanics

Abstract

Nervous systems must adapt to shifts in behavioural ecology. One form of adaptation is neural exaptation, in which neural circuits are co-opted to perform additional novel functions. Here, we describe the co-option of a motor-to-somatosensory circuit into an olfactory network. Many moths beat their wings during odour-tracking, whether walking or flying, causing strong oscillations of airflow around the antennae, altering odour plume structure. This self-induced sensory stimulation could impose selective pressures that influence neural circuit evolution, specifically fostering the emergence of corollary discharge circuits. In Manduca sexta, a pair of mesothoracic to deutocerebral histaminergic neurons (MDHns), project from the mesothoracic neuromere to both antennal lobes (ALs), the first olfactory neuropil. Consistent with a hypothetical role in providing the olfactory system with a corollary discharge, we demonstrate that the MDHns innervate the ALs of advanced and basal moths, but not butterflies, which differ in wing beat and flight pattern. The MDHns probably arose in crustaceans and in many arthropods innervate mechanosensory areas, but not the olfactory system. The MDHns, therefore, represent an example of architectural exaptation, in which neurons that provide motor output information to mechanosensory regions have been co-opted to provide information to the olfactory system in moths.

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

“…Thus, the MDHns likely influence the ability of the AL network to track odor timing and facilitate assembly of a salient “olfactory image.” Given that odor-guided behavior in M. sexta is performed primarily during flight and the MDHns originate in a flight sensory and motor pattern-generating center, we propose that the MDHns optimize olfactory function within the context of odor-guided flight. Finally, given their ubiquity across insects ( 35 ) and their projections into multiple additional sensory processing centers, we have only begun to understand the multimodal nature of MDHn’s role in coordinating wing-motor actions with sensory processing.…”

“…In most insects, the MDHns project to the subesophageal zone and antennal mechanosensory and motor center (AMMC). However, in nocturnally active plume-tracking insects, like caddisflies ( 34 ) and moths, the MDHns innervate the AL as well ( 35 ). Interestingly, this circuit appears to have been lost in closely related butterflies ( 35 ), which are diurnal and differ from moths in their flight mechanics and relative reliance on visual, rather than olfactory cues.…”

“…However, in nocturnally active plume-tracking insects, like caddisflies ( 34 ) and moths, the MDHns innervate the AL as well ( 35 ). Interestingly, this circuit appears to have been lost in closely related butterflies ( 35 ), which are diurnal and differ from moths in their flight mechanics and relative reliance on visual, rather than olfactory cues. The MDHns are therefore excellent candidates for a CDC between flight sensory motor centers in the ventral nerve cord and the olfactory system in the moth brain; however, neither their function during flight nor their functional role in olfactory processing and odor-guided behavior is known.…”

Histaminergic interneurons in the ventral nerve cord: assessment of their value for Euarthropod phylogeny

“…#22939). The same antibody has been used within several insect species, as well as a centipede and a tick [57, 70]. The total absence of immunolabeling in Drosophila null lines for histidine decarboxylase [63] indicates a high specificity of the antibody.…”

“…Recently, it was demonstrated that a single pair of mesothoracic histaminergic neurons innervate a subset of antennal lobe glomeruli in Manduca sexta [69]. This sensory-motor circuit has been identified in several moth species, but not in other insects including locusts, flies and butterflies, where these neurons build a motor-to-mechanosensory circuit [70].…”