Neuromechanism Study of Insect–Machine Interface: Flight Control by Neural Electrical Stimulation

Abstract

The insect–machine interface (IMI) is a novel approach developed for man-made air vehicles, which directly controls insect flight by either neuromuscular or neural stimulation. In our previous study of IMI, we induced flight initiation and cessation reproducibly in restrained honeybees (Apis mellifera L.) via electrical stimulation of the bilateral optic lobes. To explore the neuromechanism underlying IMI, we applied electrical stimulation to seven subregions of the honeybee brain with the aid of a new method for localizing brain regions. Results showed that the success rate for initiating honeybee flight decreased in the order: α-lobe (or β-lobe), ellipsoid body, lobula, medulla and antennal lobe. Based on a comparison with other neurobiological studies in honeybees, we propose that there is a cluster of descending neurons in the honeybee brain that transmits neural excitation from stimulated brain areas to the thoracic ganglia, leading to flight behavior. This neural circuit may involve the higher-order integration center, the primary visual processing center and the suboesophageal ganglion, which is also associated with a possible learning and memory pathway. By pharmacologically manipulating the electrically stimulated honeybee brain, we have shown that octopamine, rather than dopamine, serotonin and acetylcholine, plays a part in the circuit underlying electrically elicited honeybee flight. Our study presents a new brain stimulation protocol for the honeybee–machine interface and has solved one of the questions with regard to understanding which functional divisions of the insect brain participate in flight control. It will support further studies to uncover the involved neurons inside specific brain areas and to test the hypothesized involvement of a visual learning and memory pathway in IMI flight control.

Anopheles stephensi Feeding, Flight Behavior, and Infection With Malaria Parasites are Altered by Ingestion of Serotonin

“…In D. melanogaster , walking speed was decreased when ventral nerve cord serotonergic signaling was activated, but walking speed was increased when this signaling was inhibited ( Howard et al, 2019 ). In the honeybee Apis mellifera , however, flight behavior was not impacted by manipulation of 5-HT ( Zhao et al, 2014 ). In A. aegypti , reduced 5-HT levels were associated with increased flight distance ( Ngai et al, 2019 ).…”

Extended Flight Bouts Require Disinhibition from GABAergic Mushroom Body Neurons

“…The OA-VPM4 neurons have recently been implicated in promoting feeding initiation [39]. In honeybees, electrical stimulation of deep SEZ with high current intensity initiated flight [40]. Although the precise sensory inputs to the OA neurons remain unclear, the SEZ receives proprioceptive information regarding feeding from the head, the mouth cavity, and the trunk [41] as well as mechanosensory inputs from thoracic bristles, eye bristles, wings, and halteres [42].…”

Insect-machine Hybrid System: Remote Radio Control of a Freely Flying Beetle (<em>Mercynorrhina torquata</em>)

“…On the ground, researchers have demonstrated walking control by stimulating the neuromuscular sites of cockroaches 4,12,14 , spiders 15 , and beetles 16,17 . In the air, the initiation and cessation of flight were achieved using different methods such as the stimulation of the optic lobes (the massive neural cluster of a compound eye) in beetles 7,9 and brain sub-regions in bees 18 , whereas turning control has been demonstrated by stimulating the antennae muscles and nervous system of the abdomens in moths 11,19 and the flight muscles of beetles 7,9,13 . In most cases, a built-in radio microcontroller was integrated on a custom-designed printed circuit board to produce a miniature wireless stimulator (backpack), which was mounted on the insect of interest.…”