radio controlled cyborg beetle

Frontiers in Integrative Neuroscience www.frontiersin.org October 2009 | Volume 3 | Article 24 | 1

INTEGRATIVE NEUROSCIENCESUPPLEMENTARY MATERIAL

published: 05 October 2009doi: 10.3389/neuro.07.024.2009

Remote radio control of insect fl ight

Hirotaka Sato1*, Christopher W. Berry2, Yoav Peeri1, Emen Baghoomian1, Brendan E. Casey2, Gabriel Lavella1,

John M. VandenBrooks3, Jon F. Harrison3 and Michel M. Maharbiz1,2

1 Department of Electrical Engineering and Computer Science, University of California at Berkeley, Berkeley, CA, USA2 Department of Electrical Engineering and Computer Science, University of Michigan, Ann Arbor, MI, USA3 School of Life Sciences, Arizona State University, Tempe, AZ, USA

Edited by: Rui M. Costa, Instituto Gulbenkian de Ciência, Portugal

Reviewed by: Ty Hedrick, The University of North Carolina at Chapel Hill, USA Reid Harrison, The University of Utah, USA

*Correspondence: Hirotaka Sato, 407 Cory Hall, Department of Electrical Engineering and Computer Science, University of California at Berkeley, Berkeley, CA 94720-1776, USA.e-mail: [email protected]

Received: 18 June 2009; paper pending published: 24 August 2009; accepted: 09 September 2009; published online: 05 October 2009.

Citation: Sato H, Berry CW, Peeri Y, Baghoomian E, Casey BE, Lavella G, VandenBrooks JM, Harrison JF and Maharbiz MM (2009) Remote radio control of insect fl ight. Front. Integr. Neurosci. 3:24. doi: 10.3389/neuro.07.024.2009

Copyright © 2009 Sato, Berry, Peeri, Baghoomian, Casey, Lavella, VandenBrooks, Harrison, Maharbiz. This is an open-access article subject to an exclusive license agreement between the authors and the Frontiers Research Foundation, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.

MOVIE 1 | This movie shows initiation and cessation control of Cotinis texana

fl ight (fi rst half) and the effect of higher frequency negative and positive pulse

trains on the modulation of the wing oscillations (second half).

MOVIE 2 | This movie shows a weakly tethered (thin wire) Cotinis texana

repeatedly stimulated to start and stop fl ight.

MOVIE 3 | This movie shows representative responses of Cotinis texana

when positive and negative potential pulses were applied to the brain. At positive potential pulses, Cotinis unfolded and extended legs; negative potential pulse triggered folding of the legs. The upper LED blinked when the positive potential pulse was applied to the brain, while the lower one blinked when the negative potential pulse was applied to the brain (1000 fps, 5× speed).

MOVIE 4 | This high speed movie (500 fps) shows an untethered

microsystem-triggered fl ight initiation sequence of Cotinis texana.

MOVIE 5 | This movie shows initiation and cessation control of Mecynorrhina

torquata fl ight. A tethered beetle unfolded its wings and started wing oscillation immediately after 100 Hz pulse trains were applied between the left and right optic lobes. The beetle quickly stopped fl ight and folded its wings when a single pulse was applied.

MOVIE 6 | This movie shows initiation of fl ight and takeoff of an

unconstrained Mecynorrhina torquata beetle equipped with an RF receiver

for wireless communication. A radio command triggered the microcontroller to apply 100 Hz pulse trains between the left and right optic lobes, and then the beetle started wing oscillations and took off into the air. A red LED indicator mounted on the RF receiver showed when stimulation was commanded by remote operator.

MOVIE 7 | This movie shows a series of initiation and cessation rounds of an

unconstrained Mecynorrhina torquata beetle equipped with an RF receiver

for wireless communication. The initiation stimulus made the beetle take off into the air in the same manner as Movie 6. The beetle then stopped fl ying when a single pulse was sent to the region between the optic lobes. A red LED indicator mounted on the RF receiver showed when stimulation was commanded by remote operator.

MOVIE 8 | This movie shows elevation control of Cotinis texana on a pitching

gimbal. A beetle increased its climbing rate whenever stimulus pulse trains were applied to the brain (an LED indicator blinked). It returned to normal fl ight when un-stimulated (the LED was off).

MOVIE 9 | This high speed movie (6000 fps) shows un-stimulated and

stimulated fl ight of Cotinis texana for comparison of wing oscillation

frequency. Stimulated fl ight resulted in faster wing oscillation than un-stimulated fl ight; the stimulated fl ight started the 30th pronation at 1:19.00 in the movie while the un-stimulated one ended the 29th pronation. The frame rate of the high speed camera was approximately 85 times the wing oscillation frequency.

MOVIE 10 | This movie shows elevation control of fl ying Mecynorrhina

torquata on a pitching gimbal. The beetle decreased its climbing rate whenever stimulus pulse trains were applied to the brain (the pulse trains appeared on oscilloscope monitor). It returned to normal fl ight when un-stimulated (the pulse trains disappeared from the oscilloscope monitor).

MOVIE 11 | This movie shows remote elevation-control of free-fl ying

Mecynorrhina torquata. An RF receiver for wireless communication was mounted on the beetle. Wireless commands instructed the microcontroller to apply stimuli to the brain (see text), which caused the beetle to lose altitude. Once the command was removed, the beetle returns to normal fl ight and regains altitude. A blue LED blinked whenever the microcontroller received a command sent by remote operator.

MOVIE 12 | This movie shows turn control of fl ying Cotinis texana. The following stimuli were applied:

1) A 100 Hz positive potential pulse train was applied to basalar muscle of one side via the implanted stimulator for 2 s,

2) Two seconds pause,3) A 100-Hz positive potential pulse train was applied to basalar muscle of the

other side via the implanted stimulator for 2 s,4) Two seconds pause,5) Repeated the sequence.


Sato et al. Remote radio control of insect fl ight

This generated a sequence of turns. A right turn, for example, was triggered by stimulating the left fl ight muscle. During turning we noted that the mid leg on the stimulus side dropped down.

MOVIE 13 | This movie shows remote turn-control of free-fl ying

Mecynorrhina torquata. An RF receiver for wireless communication

was mounted on the beetle. After the RF receiver accepted a command to apply stimulus pulse trains to either left or right basalar muscle, the beetle turned. Red, green and yellow LED indicators were placed on the ground to show when the remote operator commanded the optic lobe (fl ight initiation), right basalar (left turn) and left basalar (right turn) muscle stimulations, respectively.

Table 1 | Data on stimulated fl ight bouts in individual Cotinis texana.

Insect Weight (g) Amplitude Number Total Duration τ1 (s) τ

2 (s) DN AN DP AP

threshold (V) of fl ight fl ight of a single

bouts duration (s) fl ight (s)

NEG + POS

1 1.27 3.2 13 7.9 0.5 (0.2–1.4) 0.5 (0.2–3.7) – 11 2 0 0

2 1.12 2.1 3 273.7 1.7 (1.3–270.6) 1.2 0.8 (0.8–0.9) 1 0 2 0

3 0.98 1.6 1 6.2 1.0 – 0 1 0 0

4 0.83 3.6 1 1793.1 2.0 – 0 1 0 0

5 0.90 4.7 1 177.7 0.0 – 1 0 0 0POS

6 0.90 2.9 92 774.0 2.5 (0.5–233.3) – 1.4 (0.5–1.8) – – 0 92

7 1.12 2.1 22 46.1 2.0 (1.0–3.7) – 1.0 (0.5–4.1) – – 8 14

8 0.73 3.7 6 5.4 0.6 (0.5–2.1) – 1.6 (1.4–4.8) – – 0 6

9 0.88 4.0 5 348.1 58.8 (22.0–148.6) – 1.6 (1.5–2.0) – – 0 5

Alternating positive and negative potential pulse trains (0.1 Hz, called ‘Neg + Pos’ in the fi rst column) and positive pulse trains (0.2 Hz, called ‘Pos’) were applied to the insects as described in the text and in Figure 3. For each of the two types of stimuli, nine beetles were implanted and tested as described. Four of nine and fi ve of nine beetles did not fl y in Neg + Pos and Pos protocols, respectively. For single fl ight duration, range is in parentheses and shown right next to median if applicable. Medians and ranges of response times, τ1 and τ2 are also shown in the same manner. τ1 and τ2 are defi ned in Figure 3. DN, number of fl ight bouts which began during negative pulse; AN, number of fl ight bouts which began after negative pulse; DP, number of fl ight bouts which began during positive pulse; AP, number of fl ight bouts which began after positive pulse (see Figure 3).

Table 2 | Data on stimulated fl ight bouts in individual Mecynorrhina torquata.

Insect Weight (g) Number of stimulations required Duration of a single fl ight Response time to

to trigger fl ight initiation bought (s) initiation, τ3 (s)

2.0 V 3.0 V 4.0 V 2.0 V 3.0 V 4.0 V 2.0 V 3.0 V 4.0 V

1 8.2 42 13 1 773.5 182.8 0.7 0.5 0.2 0.3

2 7.5 53 38 30 28.8 30.3 2292.1 0.6 0.6 0.5

3 8.5 25 28 29 426.0 45.5 248.5 0.3 0.6 0.8

4 7.5 – 11 10 – 18.0 34.0 – 0.2 0.4

5 8.1 9 14 14 38.8 22.4 22.9 0.3 0.8 0.6

6 7.3 30 17 23 5.9 5.6 211.6 0.6 1.4 0.4

7 8.5 21 19 17 68.7 50.8 51.5 0.2 0.3 0.2

8 8.5 48 95 91 101.7 73.7 1.0 0.5 1.3 1.1

9 7.8 15 17 17 39.6 101.1 33.3 0.3 1.0 0.6

10 7.4 21 9 8 165.1 55.0 33.0 0.4 0.2 0.3

Alternating positive and negative potential pulse trains (100 Hz) were applied to the insects as described in the text and in Figure 4. Ten beetles were implanted and tested for three different stimulus amplitudes of 2.0, 3.0 and 4.0 V. Response time, τ3 is defi ned in Figure 4. All the tests except for the case of #4 insect at 2.0 V resulted in successful fl ight initiation.



Table 3 | Data on cessation of fl ight in individual Mecynorrhina torquata.

Flight bout number

1 2 3 4 5 6 7 8 9 10

INSECT NUMBER

1 3.0 3.0 2.0 3.0 2.0 2.0 3.0 2.0 3.0 3.0

33 67 100 33 33 300 33 100 67 33

2 3.0 3.0 3.0 3.0 2.0 3.0 2.0 2.0 3.0 2.0

100 133 67 67 100 33 33 133 33 100

3 2.0 2.0 2.0 2.0 2.0 2.0 2.0 2.0 2.0 2.0

33 67 67 333 33 100 33 33 67 33

4 2.0 3.0 2.0 2.0 3.0 2.0 2.0 2.0 3.0 2.0

33 33 33 33 33 33 33 67 33 33

5 2.0 2.0 3.0 3.0 3.0 3.0 4.0 3.0 4.0 4.0

33 67 33 67 33 67 67 67 67 33

6 3.0 4.0 5.0 4.0 4.0 4.0 3.0 3.0 3.0 3.0

33 100 100 133 67 100 100 200 133 33

7 2.0 3.0 3.0 3.0 4.0 2.0 3.0 2.0 2.0 2.0

33 33 33 33 33 33 33 33 33 33

8 4.0 4.0 4.0 4.0 4.0 4.0 4.0 3.0 4.0 3.0

33 33 33 33 33 33 33 200 33 67

9 3.0 3.0 3.0 3.0 4.0 2.0 4.0 4.0 4.0 4.0

33 67 67 167 33 33 100 67 33 33

10 6.0 5.0 5.0 5.0 3.0 3.0 3.0 3.0 5.0 3.0

567 167 167 100 67 33 67 100 100 133

A single pulse was applied to the electrodes implanted into the optic lobes after the beetle started fl ight by the initiation stimulus. The amplitude was started at 2.0 V, and then it was increased by 1.0 V unless the beetle stopped the fl ight. We repeated this cycle until the beetle stopped. All the tested beetles stopped fl ight until 6.0 V. This test was repeated ten times per each beetle and we tested ten beetles in total. Amplitude stopping fl ight (V) and response time to cessation (unit: ms, defi ned as τ4 in Figure 4) are shown in the upper and lower numbers in each cell, respectively.

Table 4 | Wing oscillation frequencies at un-stimulated and stimulated

fl ights (Cotinis texana).

Frequency (Hz)

Insect Un-stimulated (fn, normal) Stimulated (f

s) Increase (%)

1 72 76 5.6

2 66 69 4.5

3 72 74 2.8

4 80 91 13.8

5 72 74 2.8

Alternating positive and negative potential pulse trains (10 Hz, 3.0 V) were applied to the insect brain as described in the text and in Figure 5. Five beetles were implanted and tested. The mean frequency calculated from ten different wing strokes is shown in each cell in the second and third columns. Increase (%) = (fs − fn)/fn × 100. Median increase was 5.6%.

Table 5 | Gimbal pitch angle change (Mecynorrhina torquata).

Insect Number of ΔθΔθ (degree) Number of tests resulting

tests in fl ight cessation

1 29 −4.42 7

2 6 −0.69 2

3 21 −3.03 5

4 17 3.61 0

5 15 −0.52 1

6 11 −4.15 7

7 21 −1.51 5

8 8 −13.04 5

9 11 −0.33 7

10 28 −0.84 1

11 5 −0.39 1

Alternating positive and negative potential pulse trains (10 Hz, 2.0 V) were applied to the insect brain as described in the text and in Figure 6. Eleven beetles were implanted, and tested using a custom pitching gimbal. Δθ is mean difference of gimbal pitch angle to horizon between un-stimulated (θn) and stimulated (θs) fl ights: Δθ = θn − θs. Negative value of Δθ indicates that the beetle climbed down when stimulated, and vice versa. Ten of eleven insects climbed down when stimulated: only the #4 insect climbed up. In some cases, the brain stimulus resulted in cessation of fl ight as shown in the fourth column.



Table 6 | Data on stimulated turns in free-fl ight Mecynorrhina torquata.

Turn Number of insects fl ying θi θ

f Inclination angle, ΔθΔθ = θ

i − θ

f Yaw angle, φ

Left 7 −7.0 (−9.9 to 19.6) −4.5 (−10.1 to 9.3) 1.7 (−18.6 to 7.7) 20.0 (16.0–27.1)

Right 5 −4.2 (−9.5 to 8.8) −14.1 (−18.5 to 5.6) −9.0 (−15.2 to 0.5) 32.4 (14.2–46.4)

Positive potential pulse trains were applied to either left or right basalar fl ight muscle. Beetle turned toward a direction opposite to stimulated side. The stimulus was set to last for 0.5 s (14–16 frames in a normal speed camera). Each fl ight trajectory was fi lmed by multiple cameras set at different corners and other positions in a closed room. The fl ight trajectory was three-dimensionally digitized in all the frames: fl ight path consisting of 14–16 plots were obtained in each fl ight trajectory. θi and θf are the angles to ground (XY-plane) of the fi rst and last vectors of fl ight path, respectively. Therefore, Δθ = θi − θf expresses inclination angle during the stimulus. Each fl ight path was transformed and projected on a plane as shown in Figure 9 (see the text for details of the method). φ is angle of the fi nal vector to the fi rst vector after the projection, which expresses yaw angle during the stimulus. Through the third to sixth columns, range is in parentheses and shown right next to median.

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FIGURE 1 | Circuit diagrams of brain stimulator (left) and muscular stimulator (center) and photograph of both stimulators (right) for Cotinis texana. (A) into posterior pronotum (counter electrode), (B) into brain, (C) into posterior pronotum (counter electrode), (D) into right basalar muscle, (E) into left basalar muscle.

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FIGURE 2 | Circuit diagram (left) and photograph (right) of RF receiver (rigid

PCB + misc components = 687 mg, dipole antenna = 74 mg,

microcontroller = 130 mg). Stimulating electrodes were soldered on output pins such as P0_0. Wires were soldered on DVDD and GND, and they were

connected to positive and negative terminals of a rechargeable micro lithium ion battery (Micro Avionics, 3.9 V, 8.5 mAh, 350 mg). The assembly of RF receiver and battery was glued and mounted on a live beetle platform with beeswax (90 mg). The total weight was then 1331 mg when the assembly was in use.



FIGURE 3 | Custom gimbal setup consists of (A) outer ring, (B) inner ring,

and (C) silicone elastomer fl exures (PDMS, polydimethylsiloxane), (D)

center pole of the inner ring. The edges were horizontally supported by lab jacks. This photo is of one used for Cotinis texana. Another relatively larger one was used for Mecynorrhina torquata.

20 mA

2.0 sec

10 %

10 %

40 %40 %

1.5 V

2.0 sec

A

B 10 %

10 %

40 %40 %

2.0 V

2.5 msec

250 mA

2.5 msec

C

D

FIGURE 4 | Representative current wave (A) monitored when potential pulses (B) were applied between brain and posterior pronotum of Cotinis texana. Representative current wave (C) monitored when potential pulses (D) were applied between left and right optic lobes of Mecynorrhina torquata.



0

1

2

3

4

5

6

7

0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6

Num

ber o

f flig

ht

Response time to flight initiation(sec)

2.0 V

3.0 V

4.0 V

FIGURE 5 | Frequency distribution of number of stimuli required to

trigger fl ight initiation in Mecynorrhina torquata at different stimulus

amplitudes of 2, 3 and 4 V.

0

2

4

6

8

10

12

0 10 20 30 40 50 60 70 80 90 100

Num

ber o

f flig

ht

Number of stimuli required to trigger flight initiation

2.0 V

3.0 V

4.0 V

FIGURE 6 | Frequency distribution of response time to fl ight initiation in

Mecynorrhina torquata at different stimulus amplitudes of 2, 3 and 4 V.

0

10

20

30

40

50

60

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

Num

ber o

f flig

htResponse time to cessation of flight

(number of frames, or 1/30 sec)

0

10

20

30

40

50

60

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

2.0 V

3.0 V

4.0 V

5.0 V

6.0 V

FIGURE 7 | Frequency distribution of response time to cessation of fl ight

in Mecynorrhina torquata at different stimulus amplitudes of 2, 3 and 4 V.



0

1

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Num

ber o

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Inclination angle (degree)

Num

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Yaw angle (degree)

0

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Left Turn

Right Turn

Left Turn

Right Turn

A

B

–90 –80 –70 –60 –50 –40 –30 –20 –10 0 10 20 30 40 50 60 70 80 90

0 10 20 30 40 50 60 70 80 90

FIGURE 8 | Frequency distributions of (A) inclination angle and (B) yaw angle (ΔθΔθ and φ in Table 6, respectively) in Mecynorrhina torquata at different

stimulus amplitudes of 2, 3 and 4 V.

radio controlled cyborg beetle

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