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.
Highlights
Insects, due to their impressive flight skills, are ranked among the best models for studying mechanisms of flight control, and for use in the development of biomimetic micro air vehicles (MAVs) [1]
The mediolateral positional data for five brain subregions were measured as perpendicular distance to the brain midline (Fig. 3A, B, C), and antero-posterior positional data were measured as perpendicular depth to the brain surface (Fig. 3C)
All data were recorded in Microsoft Excel and processed into curve charts to show the positional distribution of different subregions in the honeybee brain
Summary
Due to their impressive flight skills, are ranked among the best models for studying mechanisms of flight control, and for use in the development of biomimetic micro air vehicles (MAVs) [1]. A novel approach called the insect– machine interface (IMI), which directly controls the flight behavior of insects by either neuromuscular or neural stimulation, has been developed in recent years and promises to overcome some of the challenges facing MAVs [4,5]. The use of electrical stimulation to induce behavior in insects is not new. Blondeau (1981) had stimulated neurons in the lobula plate of free-moving and fixed Calliphora erythrocephala to evoke course control [11]. In these studies, electrical stimulation was used as one of the tools of neuroethology to investigate the relationship between animal behavior and the nervous system. Holzer and Shimoyama (1997) had induced the escape turn of cockroach via electrical stimulation to antennae, and built an electronic backpack to control cockroach walking [12]
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