Research Article | Open Access
T. Thang Vo-Doan, V. Than Dung, Hirotaka Sato, "A Cyborg Insect Reveals a Function of a Muscle in Free Flight", Cyborg and Bionic Systems, vol. 2022, Article ID 9780504, 11 pages, 2022. https://doi.org/10.34133/2022/9780504
A Cyborg Insect Reveals a Function of a Muscle in Free Flight
While engineers put lots of effort, resources, and time in building insect scale micro aerial vehicles (MAVs) that fly like insects, insects themselves are the real masters of flight. What if we would use living insect as platform for MAV instead? Here, we reported a flight control via electrical stimulation of a flight muscle of an insect-computer hybrid robot, which is the interface of a mountable wireless backpack controller and a living beetle. The beetle uses indirect flight muscles to drive wing flapping and three major direct flight muscles (basalar, subalar, and third axilliary (3Ax) muscles) to control the kinematics of the wings for flight maneuver. While turning control was already achieved by stimulating basalar and 3Ax muscles, electrical stimulation of subalar muscles resulted in braking and elevation control in flight. We also demonstrated around 20 degrees of contralateral yaw and roll by stimulating individual subalar muscle. Stimulating both subalar muscles lead to an increase of 20 degrees in pitch and decelerate the flight by 1.5 m/s2 as well as an induce in elevation of 2 m/s2.
Developing insect-inspired flapping wing micro aerial vehicles (MAVs) has drawn lots of interest from engineers in the recent decades due to the higher efficiency of insect flight as compared to traditional rotational wings [1–16]. Although great efforts and resources were expended to optimize the structural and material design of the MAVs toward untethered autonomous and endurance flight, it is still challenging to match the performance capability of the insects in terms of actuating, sensing, energy efficiency, and locomotion control. While the centimeter-scale flyers used a combination of small electromagnetic motors, linkages, and crank or pulley-string to drive the wings [4–6, 15], the millimeter-scale ones required piezoelectric actuators or soft dielectric elastomer actuators and compliant mechanisms to generate wing flapping [2, 4, 7, 8]. Tilting the whole flapping mechanism to alter stroke plane [4, 5] and generating passive wing rotation or asymmetric flapping frequencies and amplitudes [2, 4, 7, 9] were also implemented to control the flight of MAVs. Simplifying flight mechanisms due to size and weight limit makes MAVs not able to match the agile flight control of the insects as the native flyers can control wing kinematics both passively and actively by activating indirect and direct flight muscles [4, 17]. Scaling the robots to insect size also faces a bottle neck in durability of materials (e.g., actuators and chassis) that limit their life cycle significantly [2, 4, 5, 7, 9, 16]. Furthermore, free flight endurance is still a challenge as the current longest flight of flapping MAVs is less than 12 minus due to high power consumption of the actuators along with wireless communication and sensors. While it took engineers years or even decades to achieve a perfect insect-scale MAV [1–16], insects are already perfect flyers. They consist of indirect flight muscles for flapping the wings, direct flight muscles for altering wing kinematics, and resilient cuticle of thorax and wing hinges that can last for a lifetime. They also have a complex sensory and neural network for precise feedback control of motor actions. Insects have more agile maneuverability in flight as they can control wing kinematics both actively and passively to easily turn, adjust altitude, body angles, hover, and even have extreme motion like saccade [18–24]. Thus, MAV based on living insect platform would be a preferred model that inherits the insect’s high efficiency, maneuverability, and endurance in flight while bypassing complex mechanical and material design, fabrication process, and high power consumption issue [25–29].
The interface of a living insect platform and a mounted control backpack results in a resilient insect-computer hybrid robot, also known as cyborg insect, or insect biobot. The motor actions of the insect can be controlled by sending the electrical stimulus directly from the backpack terminals to the muscles or neural clusters through implanted electrodes. Precise walking gaits in beetles were achieved by stimulating the leg muscles [30, 31] while turning, backward, forward, and sideways walking were driven by stimulating the mechanosensory organs (e.g., antennae, cercus, and elytra) and ganglion in beetles [32, 33] and cockroaches [34–36]. Flight initiation and cessation of the beetles were achieved by stimulating optic lobes  and indirect flight muscles  while stimulating direct flight muscles enable steering control in flight [25, 27, 28]. In addition, there were also attempts to control moth flight by direct stimulation of insect brain areas , ventral nerve cord that controls abdominal deflection , and antennal muscles . Although various insect platforms were evaluated for MAV application, giant flower beetles were superior candidates due to not only their agile flight capability but also their firm exoskeleton to protect themselves from crashes and high payload to carry heavy backpack and battery [25–27, 29, 40]. While stimulating basalar muscles (Figure 1) increase the wing beat amplitude that cause contralateral turn , the activation of third axillary muscle (3Ax) resulted in ipsilateral turn due to decrease in wing amplitude in beetles . In addition, stimulating basalar and 3Ax muscle alternatively with a feedback control system could drive the beetle to follow a predetermined path or altitude in flight [28, 41]. Although tuning wing amplitudes for turning control of beetle flight is well established, the control of wing rotation for body angles and braking is lacking. Such capability of body angle and braking control would enable more complex maneuverability of beetle flight such as hovering, perching, and saccade.
Here, we demonstrated a stimulation protocol of subalar muscle, the last major direct flight muscle besides basalar and 3Ax muscles, to control the braking and body angles of an insect-computer hybrid robot based on a live beetle (Mecynorrhina torquata) in flight (Figures 1(a)–1(c)). During fictive decelerated flight in tethered condition, the firing rate of subalar muscle and the wing rotation angle increased which suggested the role of subalar muscle in braking and pitch control. Stimulating individual subalar muscle in free flight induced contralateral yaw and roll of the body as well as increase in pitch angles. Moreover, stimulating both subalar muscles simultaneously also resulted in braking and elevation in flight.
2. Materials and Methods
Adult Mecynorrhina torquata beetles (6 cm–8 cm, 8–10 g) were imported from Kingdom of Beetle, Taiwan, and reared in separate containers ( cm) with woodpile beading. They were fed sugar jelly every 3 days. The temperature and humidity of the rearing room were maintained at 25°C and 60%. Invertebrates, including beetles, does not require ethics approval for animal research according to the National Advisory Committee for Laboratory Animal Research.
2.2. Electrode Implantation
Beetles were anesthetized for 3 min in a small CO2-filled container. The beetle was then placed on a wooden block and gently covered with dental wax, which was presoftened by dipping into hot water. Two silver wire electrodes (diameter of the bare wire, 127 μm, and diameter of the coated wire, 178 μm; A-M Systems) were implanted into the subalar muscle at a depth of 3 mm through a small opening on the cuticle. Before the electrodes were inserted, the bare silver was exposed by flaming. The electrodes were secured in place by melted beeswax.
2.3. Wireless Backpack Assembly
The wireless system included two electronic devices that were based on the TI CC2431 microcontroller . One was the miniature wireless backpack, which was mounted onto the beetle, and the other was the base station connected to the computer. The backpack was driven by a micro poly lithium-ion battery (Fullriver, 3.7 V, 350 mg, 10 mAh) wrapped with retro-reflective tape (Silver-White, Reflexite), which also served as a marker for the motion capture system. The total mass of the backpack, including the battery, was g. The additional mass from the backpack has minimal effect on beetle flight speed. The backpack mounted beetles behaved as close as load-free beetle while excessive load significantly decreased the velocity of the beetle flight (Figure 1 and S1).
An IMU backpack was used to record the body angles and accelerations of the flying insect. The backpack contains a nine axis IMU MPU9250 from InvenSense to measure orientation and movement of the board and the BLE microcontroller CC2642R from Texas Instrument. The IMU integrates a small digital computational engine to do sensor fusion from its nine axes of data sensor which 3-axis acceleration, 3-axis gyroscope, and 3-axis magnetometer. The IMU sensor results in three linear accelerations and the sensor orientations in quaternion format. The IMU was sampled with sampling rate 100 Hz. The total mass of the backpack, including the battery, was g.
2.4. Tethered Experiment
The beetle was placed within the field of view of six near-infrared cameras (VICON T40s) in the three-dimensional (3D) motion capture system (Figure 2(a)) to record wing kinematics. Retro-reflective markers were attached to the wings and body of the beetle (Figure 2(b)); then, the silver wire electrodes were implanted into the subalar muscle and connected to the EMG recorder (CC2431 Microcontroller Development board) through an instrument amplifier (Analog Devices, LT1920) or a function generator. For visual stimulation, a visual stimulator was set to project the optic flow pattern (vertical black/white stripes of 20 mm) onto two monitors placed 250 mm in front of the beetle (Figures 2(c) and 2(d)). When the patterns moved, the beetle changed the wing kinematics to track the moving patterns. The EMG signal was recorded from the subalar muscle and synchronized with the wing kinematics (Figure 2(e)). For electrical stimulation, the wing kinematics were synchronized with the electrical stimulus. Change in wing stroke plane is not considered as activating subalar muscle does not alter wing stroke plane .
2.5. Free Flight Experiment
The experiment was conducted in a flight arena of m covered by a motion capture system equipped with 20 near-infrared cameras (VICON, T40s, and T160). After assembly, the wireless connection to the backpack and operation laptop was set up. The beetle was then released into the flight arena and stimulated via a Wii remote. Activation of the Wii remote sent a command to the BeetleCommander running on the laptop, which sent a wireless command to the backpack via the base station. After receiving the command, the backpack generated the electrical stimulus signal and applied it to the subalar muscle. The beetle position was recorded simultaneously by the 3D motion capture system or the IMU data is then synchronized with the electrical stimulation. The work flow of free flight stimulation experiment is shown in Figure 3.
A 500 ms pulse train was applied on the subalar muscle in free flight for electrical stimulation. The pulse amplitude and pulse width are 3 V and 3 ms, respectively (Figure S2). The stimulation frequency is varied from 40 Hz to 100 Hz. The stimulation parameters were selected from a brief survey at the beginning of the experiment setup and limited to the most effective range due to the constrain of flight duration of the beetles. Besides, the electrical stimulation of subalar muscle does not affect other nearby muscles (Figure S3).
The free flight trajectories of the beetles were sorted to individual flight paths of 150 ms before stimulation and 500 ms during stimulation. The , , and components of the velocity and acceleration were calculated after smoothing the flight path using a 5th order polynomial function by a customized MATLAB code ( beetles, trials, trials, trials). Saccade flight paths whose angular velocities were over 500°/s were excluded from the data analysis because such a fast motion could not be accurately detected. The horizontal and lateral vectors were calculated for every pair of points along the flight path on the (, ) plane. The horizontal and lateral accelerations were calculated by summing the projected and accelerations relative to the horizontal and normal vectors, respectively. The vertical acceleration is the component of the acceleration.
The IMU data was collected from different beetles ( beetles, trials, trials, trials). A 5th order Butterworth filter with cutoff frequency of 20 Hz was applied for acceleration data. The induced amount is defined as the difference of the peak value within first 300 ms during stimulation and the onset value.
2.6. Statistical Analysis
The paired sample -test was performed to check the significance of the beetle responses before and during stimulation. The one simple -test was used to check if the induced acceleration or angle was significant. Spearman correlation test was used to check the significance of the graded responses. A value less than 0.05 was considered statistically significant.
3.1. The Role of Subalar Muscle
The beetle subalar muscle is inserted from the hind leg coxa to the apodema of the subalar sclerite [20, 24]. The subalar muscle lies next to the basalar muscle at the posterior end of the thorax (Figures 1(d) and 1(e)). Its function would be similar to those of the III1 muscle of the blowfly [41, 42], M99 and M129 muscles of the locusts [26, 43–45] due to similarity in configuration. Anatomically, the contraction of the subalar muscle pulls the posterior part of the wing base, consequently, and depresses the trailing edge of the wing that increases the wing rotation angle and thus the wing angle of attack. This would lead to a decrease in thrust and increase in lift generated by the wings of the flying insect [42–45]. Such change in thrust and lift of the wings would alter the body angles or induce brake in flight [21, 42–46].
The beetle subalar muscle was innervated in a graded fashion under tethered condition. It was more active during fictive decelerating flight than nonstimulated flight (Section 2.4). During flight, we observed that the subalar muscle was continuously active (Figure 4(a)). We provided optic flow stimuli to induce fictive decelerating flight in tethered beetles [23, 45, 47]. The firing rate of the electromyogram (EMG) spike during fictive decelerating flight was higher than that during no stimulation (Figure 4(b)) (, paired sample -test). This would suggest that the beetle increases the activity of subalar muscle during braking in flight.
Whether stimulated due to fictive backward visual stimuli (Figure 5(a)) or via direct electrical stimulation (Figure 5(b)), enhanced activity in the subalar muscle caused increase in wing rotation angle. Compared to spontaneous flight (black traces, Figure 5(a)), the wing rotation and elevation angles, respectively, increased during fictive decelerating flight, with only slight changes in the corresponding deviation angle (, , , paired sample -test). Similar to braking in flight, electrical stimulation of subalar muscle led to the increment in wing rotation and elevation angles (Figure 5(b)) while little change was observed in the deviation angles (, , , paired sample -test). These results would suggest that the beetle activates subalar muscle to increase wing rotation angle when braking in flight.
3.2. Body Angles Control of the Insect-Computer Hybrid Robot in Free Flight
In free flight, the beetle with mounted IMU backpack enabled us to record body angles and accelerations of the insect during flight (Figures 6(a)–6(c)). Stimulating either left or right subalar muscle also results in increase in pitch angle from 5 degrees to 22 degrees with a weak correlation with stimulation frequency (, , Spearman correlation test; linear regression: ) (Figure 6(d)). The increase in pitch angle was from 10 degrees to 22 degrees (, , Spearman correlation test) and fitted by a linear regression (, R = 28.28%) when both subalar muscles were stimulated while there is slight change in yaw and roll angles. Such increase in pitch angle would be the result of the induced lift of the wing during the stimulation which is similar to that found in Drosophila [43, 45, 48]. Stimulating individual subalar muscle led to graded contralateral increase in yaw angle from 2 degrees to 17 degrees (, , Spearman correlation test; linear regression: ) and roll angle from 5 degrees to 10 degrees (, , Spearman correlation test; linear regression: ) when the stimulation frequency was tuned from 63 Hz to 100 Hz (Figures 6(e) and 6(f)). The change in body yaw and roll angles would be due to the asymmetry of the wing rotation angles during the stimulation. The electrical stimulation of subalar muscle would increase the wing rotation angle that lead to the increase in lift of that side . Such increases are associated with the increase in vertical acceleration and decrease in horizontal acceleration of the beetle during flight.
3.3. Braking Control of the Insect-Computer Hybrid Robot in Free Flight
A decrease of 0.7 m/s2 to 1.4 m/s2 of horizontal acceleration (Figure 6(g)) and increase of 1 m/s2 to 1.6 m/s2 of vertical acceleration (Figure 6(h)) were observed when stimulating both subalar muscles. The increase in induced lateral acceleration of 0.5 m/s2 to 1 m/s2 when individual subalar muscle was stimulated would be a side slip (Figure 6(i)). There is decrease in horizontal acceleration and increase in vertical acceleration when individual subalar muscle was stimulated but without a clear trend of change (Figures 6(g) and 6(h)). In addition, the induced yaw angle has a moderate negative correlation with the induced roll angle (, , Spearman correlation test), which is similar to that of a bank turn observed in Drosophila [15, 21] (Figure 7(a)). The increase in pitch angle is associated with the elevation during flight (, , Spearman correlation test) (Figure 7(b)). The induced horizontal acceleration and lateral acceleration have a weak correlation coefficient of -0.13 and -0.29 with the induced pitch and induced roll, respectively (, Spearman correlation test) (Figures 7(c) and 7(d)). These correlations are also in agreement with those observed in Drosophila [43, 45]. These findings support our hypothesis that the subalar muscles have a function of controlling brake, elevation, and body angles of the beetles during free flight.
In addition, recorded positions of freely flying beetles showed the same tendency observed with IMU backpack. The stimulation of the subalar muscles leaded to the decrease in horizontal acceleration and increase in vertical acceleration (Figures 8(a) and 8(b)). The induced acceleration was computed from the free flight path data (refer to “Free Flight data analysis” and ). During free flight, we also found that the induced horizontal acceleration was negative (Figure 8(b)) and gradually reduced to −1.6 m/s2 with a moderate dependence on the stimulation frequency (, , Spearman correlation; linear regression: ). In addition, stimulation of the subalar muscle induced a relatively small but significant 0.5 m/s2 to 1 m/s2 increase in the induced vertical acceleration (, one sample -test) (Figure 8(c)). Stimulate left or right subalar muscle caused an increase in induced lateral acceleration of about 0.8 m/s2 to 1.5 m/s2 ipsilaterally when the stimulation frequency is within 70 Hz to 100 Hz (, one sample -test) (Figure 8(d)). The decrease in the horizontal directions and increase in the vertical directions of the induced accelerations indicate the increase in drag and lift of the wings.
Our data showed that the role of subalar muscle in beetle flight is different from that of basalar and 3Ax muscles. While the activation basalar and 3Ax muscles cause increment and reduction in wing beat amplitude, respectively [25, 27], activating subalar muscle leads to an increase in wing rotation angle. In addition, we found that activating subalar muscle in free flight induced change in body angles and braking which are distinct from the steering role of basalar and 3Ax muscles.
Although there are graded responses of the pitch, yaw, roll, and horizontal acceleration of the beetle to electrical stimulation frequency, the low regression correlation is a potential issue for precise locomotion control with subalar muscle. Closing the control loop with feedbacks from IMU and motion capture data would improve the flight control. Despite of several attempts to implement feedback control for freely flying beetles, it is still a challenge to realize autonomous flight of insect-machine hybrid robot [28, 41]. It would be useful to have a detail physiology investigation on the role of individual flight muscles in control of wing kinematics [49–51]. Such data would provide more insight of how the individual flight muscles work and their effect in flight and thus suggest appropriate stimulation protocol to control the flight muscles. For instance, the phasic activation pattern of a muscle would suggest the efficient stimulation timing of such muscle.
Recording activities of multiple muscles and high-resolution images of the wings in tethered condition is convenient and would provide certain relationship of muscle activation and wing kinematics [49, 50, 52, 53]. However, the behavior of insects in such constrained condition would differ from freely moving ones, and it is impossible to achieve complex behaviors of the insect such as hovering and perching in such condition. While a large-scale virtual reality system can help to reproduce complex behaviors of freely flying insect , free flight EMG recording of flight muscles [55–57] along with high-resolution recording of the wings and body [21, 58–60] would provide precise correlation of muscle activation patterns and flight maneuvers. Implementing such data into a feedback control system would enable autonomous flight of insect-machine hybrid robots in the future.
Fully control the beetle flight requires the ability to activate multiple flight muscles. In this paper, we demonstrated that the role of subalar muscle in manipulating wing rotation angle which differs from regulating wing beat amplitude of basalar and 3Ax muscles. We were then able to control braking and lift as well as body angles of a beetle in free flight by activating subalar muscle. A feedback control system with the capability to stimulate all direct flight muscles would enable complex maneuver control of the beetle flight in the future.
All data needed to evaluate the conclusions in the paper are present in the paper or in the Supplementary Materials.
Conflicts of Interest
The authors declare no competing or financial interests.
T.T.V.-D. and H.S. designed the research. V. T. D. designed the hardware and software for IMU backpack. T.T.V.-D. conducted the experiments, analyzed, and interpreted data. T.T.V.-D. and H.S. wrote the paper.
The authors would like to thank Mr. Duc Long Le, Mr. Huu Duoc Nguyen, and Dr. Li Yao for the discussion and Mr. Roger Tan Kay Chia, Mr. Chew Hock See, and Mr. Seet Thian Beng for their support. This work was partly supported by the Singapore Ministry of Education (RG140/20) and SPring-8 in Japan with the approval of the Japan Synchrotron Radiation Research Institute (Nos. 2015A1502, 2015B1449, 2016A1169, 2016B1492, 2017A1087, 2017B1464, 2018A1087, and 2018B1261).
Supplementary 1. Figure S1: the flight speed of beetle with different loads. Figure S2: stimulation waveform and electrical current flow through the subalar muscle. Figure S3: EMG of nearby muscles during the electrical stimulation of the subalar muscle.
Supplementary 2. Movie S1: the response of the beetle due to electrical stimulation of subalar muscle.
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