locomotion control of hybrid cockroach...

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rsif.royalsocietypublishing.org Research Cite this article: Sanchez CJ, Chiu C-W, Zhou Y, Gonza ´lez JM, Vinson SB, Liang H. 2015 Locomotion control of hybrid cockroach robots. J. R. Soc. Interface 12: 20141363. http://dx.doi.org/10.1098/rsif.2014.1363 Received: 12 December 2014 Accepted: 6 February 2015 Subject Areas: bioengineering, biometeorology, mathematical physics Keywords: biotechnology, hybrid robotics, insect control Author for correspondence: Hong Liang e-mail: [email protected] Present address: Department of Plant Science, California State University Fresno, Fresno, CA 93740-8033, USA. Electronic supplementary material is available at http://dx.doi.org/10.1098/rsif.2014.1363 or via http://rsif.royalsocietypublishing.org. Locomotion control of hybrid cockroach robots Carlos J. Sanchez 1 , Chen-Wei Chiu 1 , Yan Zhou 1 , Jorge M. Gonza ´lez 2,† , S. Bradleigh Vinson 2 and Hong Liang 1 1 Department of Mechanical Engineering, Texas A&M University, College Station, TX 77843-3123, USA 2 Department of Entomology, Texas A&M University, College Station, TX 77843-2475, USA Natural systems retain significant advantages over engineered systems in many aspects, including size and versatility. In this research, we develop a hybrid robotic system using American (Periplaneta americana) and discoid (Blaberus discoidalis) cockroaches that uses the natural locomotion and robust- ness of the insect. A tethered control system was firstly characterized using American cockroaches, wherein implanted electrodes were used to apply an electrical stimulus to the prothoracic ganglia. Using this approach, larger discoid cockroaches were engineered into a remotely controlled hybrid robotic system. Locomotion control was achieved through electrical stimulation of the prothoracic ganglia, via a remotely operated backpack system and implanted electrodes. The backpack consisted of a microcontroller with integrated trans- ceiver protocol, and a rechargeable battery. The hybrid discoid roach was able to walk, and turn in response to an electrical stimulus to its nervous system with high repeatability of 60%. 1. Introduction The development of autonomous robotic systems has been of great interest to scientific and engineering communities [1–3]. Researchers have studied the rapid and agile locomotion that is commonly performed by different animals, particularly insects, as models for robotic systems [1,4–7]. By mimicking the control mechanisms and physical structures of natural biological systems, engineers are able to design mechanical robotic systems to optimize their performance [2,8,9]. Hybrid robotic systems using insects have attracted par- ticular attention in recent years [10,11]. The goal of those studies has been to remotely control insects with the purpose of taking advantage of their natural movements [2,8,9,12]. However, establishing efficient control of the natural leg movements of living insects has proven to be a difficult task [10,13,14]. One of the effective approaches was used by Holzer & Shimoyama [6], who observed the reaction of living insects to electrical stimulation. Through the use of controlled electrical stimulation applied to a cockroach’s nervous system, the researchers observed reactions similar to those seen under natural conditions in the roach while in the presence of a predator. A backpack system was thus developed to generate electrical stimuli transmitted through wires implanted in the antennal sockets of a cockroach. Using this method, researchers were able to obtain some level of control of walking direction by taking advantage of the roach’s natural tendency to move away from sensory data received through their antennae [15]. However, reduced responsiveness was observed as the roach appeared to become habituated to the stimuli. Habituation is a problem as the tissue often becomes less responsive over time, and the roach learns to ignore artificial stimuli [5,12,15,16]. Studies have been performed to understand and alleviate the tissue trauma when using neuro-stimulators [5,16,17]. To date, new materials and electronic systems have provided new interest for alternative methods. A better level of control and response of robotic systems must be developed in order to improve the overall performance of such a system. We report the development of a & 2015 The Author(s) Published by the Royal Society. All rights reserved. on June 13, 2018 http://rsif.royalsocietypublishing.org/ Downloaded from

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rsif.royalsocietypublishing.org

ResearchCite this article: Sanchez CJ, Chiu C-W, Zhou

Y, Gonzalez JM, Vinson SB, Liang H. 2015

Locomotion control of hybrid cockroach robots.

J. R. Soc. Interface 12: 20141363.

http://dx.doi.org/10.1098/rsif.2014.1363

Received: 12 December 2014

Accepted: 6 February 2015

Subject Areas:bioengineering, biometeorology, mathematical

physics

Keywords:biotechnology, hybrid robotics, insect control

Author for correspondence:Hong Liang

e-mail: [email protected]

†Present address: Department of Plant Science,

California State University Fresno, Fresno,

CA 93740-8033, USA.

Electronic supplementary material is available

at http://dx.doi.org/10.1098/rsif.2014.1363 or

via http://rsif.royalsocietypublishing.org.

& 2015 The Author(s) Published by the Royal Society. All rights reserved.

Locomotion control of hybridcockroach robots

Carlos J. Sanchez1, Chen-Wei Chiu1, Yan Zhou1, Jorge M. Gonzalez2,†,S. Bradleigh Vinson2 and Hong Liang1

1Department of Mechanical Engineering, Texas A&M University, College Station, TX 77843-3123, USA2Department of Entomology, Texas A&M University, College Station, TX 77843-2475, USA

Natural systems retain significant advantages over engineered systems in

many aspects, including size and versatility. In this research, we develop

a hybrid robotic system using American (Periplaneta americana) and discoid

(Blaberus discoidalis) cockroaches that uses the natural locomotion and robust-

ness of the insect. A tethered control system was firstly characterized using

American cockroaches, wherein implanted electrodes were used to apply an

electrical stimulus to the prothoracic ganglia. Using this approach, larger

discoid cockroaches were engineered into a remotely controlled hybrid robotic

system. Locomotion control was achieved through electrical stimulation of the

prothoracic ganglia, via a remotely operated backpack system and implanted

electrodes. The backpack consisted of a microcontroller with integrated trans-

ceiver protocol, and a rechargeable battery. The hybrid discoid roach was able

to walk, and turn in response to an electrical stimulus to its nervous system

with high repeatability of 60%.

1. IntroductionThe development of autonomous robotic systems has been of great interest to

scientific and engineering communities [1–3]. Researchers have studied the

rapid and agile locomotion that is commonly performed by different animals,

particularly insects, as models for robotic systems [1,4–7]. By mimicking the

control mechanisms and physical structures of natural biological systems,

engineers are able to design mechanical robotic systems to optimize their

performance [2,8,9]. Hybrid robotic systems using insects have attracted par-

ticular attention in recent years [10,11]. The goal of those studies has been to

remotely control insects with the purpose of taking advantage of their natural

movements [2,8,9,12]. However, establishing efficient control of the natural

leg movements of living insects has proven to be a difficult task [10,13,14].

One of the effective approaches was used by Holzer & Shimoyama [6], who

observed the reaction of living insects to electrical stimulation. Through the

use of controlled electrical stimulation applied to a cockroach’s nervous

system, the researchers observed reactions similar to those seen under natural

conditions in the roach while in the presence of a predator. A backpack

system was thus developed to generate electrical stimuli transmitted through

wires implanted in the antennal sockets of a cockroach. Using this method,

researchers were able to obtain some level of control of walking direction by

taking advantage of the roach’s natural tendency to move away from sensory

data received through their antennae [15]. However, reduced responsiveness

was observed as the roach appeared to become habituated to the stimuli.

Habituation is a problem as the tissue often becomes less responsive over

time, and the roach learns to ignore artificial stimuli [5,12,15,16]. Studies have

been performed to understand and alleviate the tissue trauma when using

neuro-stimulators [5,16,17]. To date, new materials and electronic systems

have provided new interest for alternative methods. A better level of control

and response of robotic systems must be developed in order to improve

the overall performance of such a system. We report the development of a

10 mm

Figure 1. Discoid cockroach with attached electronic backpack (battery ontop, board attached to the forewings). The electrodes enter the body throughthe pronotum. (Online version in colour.)

1

2R

3

4

Figure 2. Example of a typical turning experiment using a tethered Americancockroach. The image shows a left turn controlled by electrical stimulation.The wire electrodes and leash are seen as dark lines in the image. Thepath of the roach is mapped by superimposing an axis at the start position,then marking its location at 0.5 s intervals. The initial turning radius is com-puted by fitting a circle of radius R to the starting curvature of the path.(Online version in colour.)

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new approach to using electrical stimulus to control cock-

roaches’ movements. Significantly improved repeatability

and consistency in response were achieved.

In order to effectively control the movements of a cock-

roach through electrical stimulation, it was clearly necessary

to understand the complex behaviour of the nervous system

of the roach, including stimulation of ganglia and motor

neurons [18,19]. We have recently studied cockroach control

mechanisms through in vivo and in vitro antennae and cerci

stimulation with American cockroaches [11,12]. Those

works have successfully demonstrated that antenna, antennal

sockets and cerci stimulation are viable means of control but

they are not as effective as previously found [5,6,15]. Further-

more, in all reported cases it was shown that the test roaches

become conditioned to the stimuli and begin to ignore the

sensory feedback after a few trials. Locomotion control will

last only for short periods of time until it ceases all together

[6,14,15]. Methods used to control a cockroach through

implanting electrodes in antenna sockets essentially work

by tricking the roach into ‘sensing’ an obstruction which it

then tries to move away from. Stimulating the right antenna,

the roach will ‘think’ an object or a threat is present on its

right side and attempt to move away from it to the left. It

is worth noting that prior research has also shown that cock-

roaches can be conditioned to trail certain odours, and thus

the antennae seem to be highly susceptible to conditioning

[11]. That is, the roach will tend to ignore sensory feedback

from the antenna based on information gathered from other

senses. This is the primary limitation to stimulating sensory

channels such as antenna and cerci; the stimulation can only

trick the roach for so long until it learns to ignore it. In the cur-

rent study, a novel approach of locomotion control through

ganglia stimulation was accomplished through precise place-

ment of electrodes and manipulation of electrical signals

applied to the nervous system. Directly stimulating the nervous

system allows for more direct control of the cockroach’s natural

movements and eliminates the issue of conditioned behaviour.

Electrical signals were delivered through a wireless electronic

backpack attached to the cockroach, allowing for remote con-

trol of locomotion. Stimulating certain ganglia will affect

the legs attached to a particular segment of the roach. As the

roach walks or runs, its normal gait may be disrupted by apply-

ing an electrical signal to a particular nerve cluster. The

stimulation will cause a particular leg to become out of phase

with the normal gait, thereby causing a turning motion in a

desired direction.

Hybrid robotic systems have significant advantages over

conventional engineered robotic systems. Hybrid systems using

living insects that are small, have an efficient sensory system,

and respond to their environments through multiple feedback

channels. Such living systems can be self-powered through

in-taking water, air and food. These hybrid robots utilize the

behaviours of insects combined with electronics, and can be

used in many applications where conventional robots cannot

be efficiently employed. Hybrid insect robots are expected to

enable new advances in deployment, search and rescue, and

information gathering operations. They will benefit areas such

as homeland security, emergency services, construction and

mining. The uniqueness of this research is in the integration of

robotic systems with a living organism as a platform. The knowl-

edge gained will be used to integrate the two systems, resulting in

acontrollable hybrid robot that maintains the unique attributes of

a living and responsive biological system.

2. ResultsThe backpack used for wireless control consisted of a small

printed circuit board (PCB), wire electrodes and a rechargeable

lithium polymer battery. The low profile circuit board weighs

1.4 g and is 16.5 mm square. The circuit board contained

small female header pins for insertion of the electrodes.

A rechargeable lithium polymer battery (3.7 V, 50 mAh) was

used as the power source and weighed 1.5 g. The entire

system (circuit board with electronic components, battery, con-

necting wires and implant electrodes), weighed approximately

3.0 g. The complete backpack system can be seen placed on a

discoid cockroach in figure 1.

Tethered and remote-controlled experiments were recorded

using an overhead digital camera. The resulting locomotion of

the cockroaches was then analysed using imaging software

to obtain the consistency in response, and to plot the path

taken for an initiated turn. Figure 2 illustrates a typical left

initiated turn for a tethered American cockroach. For any given

experiment, the cockroach will tend to move in various direc-

tions and at various angles along its walking path. Therefore,

only the initial movements after the applied stimulation was

measured and used as a baseline for the remote-controlled exper-

iments. The initial turning movements were quantified by

50

20

40

60

80

100

120

140

160

180

10frequency (Hz)

1 V (monopolar)

left turns

right turns

initi

al tu

rnin

g ra

dius

(m

m)

15 20

Figure 3. Plot of the measured turning radius for 20 trials using 10 tethered American cockroaches for a constant 1 V signal and varied frequency. Increasing thefrequency will reduce the initial turning radius, leading to sharper turns. (Online version in colour.)

1.00

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120

1.5monopolar stimulation (V)

20 Hz stimulation

left turns

right turns

initi

al tu

rnin

g ra

dius

(m

m)

2.0 2.5

Figure 4. Plot of turning radius for 20 trials using 10 tethered American cockroaches for a constant 20 Hz signal with varied output voltage. The turning radiusbecomes smaller with increased voltage, leading to sharper turns. (Online version in colour.)

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superimposing an axis with the origin at the roach’s start pos-

ition, then mapping out its movements at 0.5 s intervals in the

lateral and vertical directions. The turning radius was determined

by superimposing a circle that best fit the initial curvature of the

path. The measurement process is illustrated in figure 2. The

controllability of a roach, in terms of success rate, was subjectively

rated based on user observation. If the user was able to success-

fully have the cockroach turn in a desired direction, then a run

was deemed successful. Numerous successful runs dictated a

roach that exhibited consistent responses.

The turning radii results for the tethered experiments invol-

ving the American cockroaches can be seen in figures 3 and 4.

For these trials, 10 cockroaches were stimulated to turn 10 times

to the left and 10 times to the right, for a total of 20 trials. The

average testing time for all roaches was approximately 45 min

to complete each trial. This time does not reflect time of consist-

ency in response, but the time required to collect the 20 data

points. Each roach was allowed to rest for at least 2 min

between each trial. The purpose of the tethered experiments

was to gain a better understanding of the electrical signal

characteristics that were necessary for optimum control.

Figure 3 shows the turning radius after applying a 1 V,

monopolar signal, a signal with a stable state of 0 V and a

varying state of higher voltage, to the cockroach ganglia at

increasing frequencies. The results show that the turning

radius decreases (i.e. sharper turns) as the frequency of the

input signal increases. Based on these results, an investigation

was carried out on the frequency that elicited the sharpest turn-

ing radius, 20 Hz. Figure 4 shows the turning radius after

applying a 20 Hz signal at increasing voltage. The results

show that the turning radius decreases as the voltage increases.

However, stimulation frequency appeared to be the more

effective control parameter than that of input voltage. The

output signal can be set at a constant low voltage (1 V),

which will reduce power consumption and increase the life

of the electronic backpack. This trend coincides with results

obtained in our previous studies involving American cock-

roaches walking on a trackball system [12]. The overall

success rate of initiating and sustaining a turn in a desired

direction (i.e. left or right turns) was approximately 70%. The

remaining 30% of trials were unsuccessful in regard to roaches

not moving when stimulated, turning in the wrong direction

or moving without turning in either direction. The signal

characteristics of the tethered study were then applied to the

start position(X0, Y0, 0 s)

(X1, Y1, 0.5 s)

X

Y

(X2, Y2, 1 s)

end areaposition(Xf, Yf, tf)

Figure 5. Turning movements were tracked by superimposing an axis at theroach’s start position. The roach was then mapped out over the axes at 0.5 sintervals to obtain the path. The solid circle on the backpack indicates themeasurement point. (Online version in colour.)

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remote-controlled experiments using the larger discoid

cockroach. A constant input voltagewas chosen, while the stimu-

lation frequency was chosen by the user during the course of a

trial. The signal used was 2.5 V, and a frequency range of

1–20 Hz was implemented in order to obtain an optimum turn-

ing during each trial. Using this methodology, a roach should

make sharper turns at higher frequency stimulation, and wider

turns at lower frequencies.

Discoid cockroaches, with an electronic backpack attached

were allowed to walk/run freely while a researcher attempted

to control the directionality of its movements. A total of three

users were given an opportunity to control a tethered and a

remote cockroach over the course of this study. Controllability

was determined by how well the user was able to initiate a turn

in the cockroach as it walked or ran across the floor. The goal of

these experiments was to test the responsiveness of the roaches

to the varied electrical stimulus. Applying a controlled electri-

cal stimulus to the pro-ganglion elicits movement in the first set

of legs in the roach. This will cause the contralateral leg to

become out of phase with the normal gait of the roach,

which will initiate a turning motion. Stimulating the right

side of the ganglion initiated turning to the left direction by

the cockroach. Similarly, left side stimulation initiated turning

to the right direction. In addition, it was found that any mono-

stable signal above 2 V applied for a long period will cause the

cockroach to stop walking or running. Application of another

asymmetric signal will re-initiate movement. All test trials

were recorded by an overhead digital camera, and later evalu-

ated with imaging software. The researcher operating the

controls attempted to manoeuvre the cockroach left and right

during any given test. A total of 20 trials were performed on

each roach, attempting to induce 10 left turns and 10 right

turns. The goal of each trial was to make the roach turn into

a pre-determined area on the right or left side of a central

axis. Controlling the roach to turn into this area, regardless of

path taken, signified a successful trial. The maximum area

seen by the overhead camera was marked off with tape to act

as a bounding box for the experiments. No other form of indi-

cator was used within the experimental area so as to not

influence the roach’s movements. At the start of each trial, a

researcher would place the roach towards the bottom of the

test area, and close to the centre line. He would then attempt

to control the roach to turn into a pre-designated area. This

area is a 75 mm circle that is centred approximately 200 mm lat-

eral and 300 mm vertical to the roach’s initial position. This is

an arbitrary area and was physically marked by the researchers

using small blocks placed on the outside of the testing area.

A trial was deemed successful if the roach was controlled to

move into this area. A trial was determined to be unsuccessful

if a roach did not move when a stimulus was applied, not turn-

ing in the intended direction, or moving forward without

turning. Each roach was allowed to rest for 3 min between

trials, and then made to turn in the opposite direction of the

previous trial. Since each roach behaved differently during test-

ing, the total experiment for each roach took an average of 1 h.

The path taken by a roach for each trial was then mapped

out using imaging software to superimpose an axis at the

start position and measuring locations at 0.5 s intervals. The

initial response time, and the average speed for each run

were also determined. The general test set-up and method-

ology for mapping the path taken by each roach is shown in

figure 5. Figures 6 and 7 show the path lines for one roach

(R1) turning left and right, along with the initial response

times and average speed for each trial. The paths taken by

this roach over the numerous trials are varied in pattern,

which was similarly observed for all the roaches. Likewise,

the amount of time that it takes for the roach to respond to

the initial stimulus at the start of the tests tends to increase

over the number of trials. The reduced responsiveness over

time was observed for all roaches tested. However, the average

speed of the roach over the numerous trials did not exhibit a

trend. The velocity for all roaches was varied, and each roach

had varied velocities over all trials. The overall success rate

using the remote backpack system was approximately 60%,

meaning that the researcher was able to control the roach

into the designated area six times out of 10. The success rate

for each of the roaches tested can be seen in figure 8, with R1

being the roach whose path lines are plotted in figures 6

and 7. It was observed that each of the roaches remained

responsive throughout the course of the hour-long experiment.

Statistically, controlling a roach to turn left had a higher success

rate than turning right (63%+4.8 versus 56%+15.0).

Once the 20 trials were completed, approximately 1 h, the

operator would continue to attempt to control the roach in var-

ious directions and to follow various paths. It was observed

that over time, the roaches tended to become fatigued and

would become unresponsive. The fatigue was brought about

by the excessive locomotion of the roach and the repeated

electrical stimulation. After a brief 10 min rest period, the

roach was able to be controlled again. A roach could typically

be controlled for time periods ranging from 30 min to 1 h

beyond the initial 1 h experiment. Therefore, using the method-

ology presented here, a cockroach can be controlled for up to 2 h.

Once initial experimentation was completed, the roach was

placed back with the colony and not tested again. Future work

will include experimentation with the same roach over different

time periods to establish longevity. One factor for loss of control

was the electrodes shifting out of position owing to the move-

ment of the roach or shifting of the backpack. This minor issue

can be alleviated through use of stronger adhesives at the

pronotum–electrode interface. The other cause for control loss

5000

trial 1

trial12345678910

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no responseno response

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00

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time (s)initial response

(mm s–1)avg. speed

trial 3trial 4trial 7

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trial 9trial 1050

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Figure 6. Plot of left paths taken for one roach (R1) over 10 trials. Initial response time to stimulation, and average speed for each trial are tabulated to the right.For trial 4, control was considered a failure as a left turn was not initiated. (Online version in colour.)

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time (s)initial response

(mm s–1)avg. speed

trial 4

trial 6

trial 7

trial 8trial 9trial 10

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Figure 7. Plot of right paths taken for one roach (R1) over 10 trials. Initial response time to stimulation and average speed for each trial are tabulated to the right.For trials 4 and 7, control was considered a failure as a right turn was not initiated. (Online version in colour.)

R10

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right

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Figure 8. Plot showing the overall rate of success for controlling 10 discoid cockroaches to turn left or right for 10 trials on each side; the average rate ofcontrollability was about 60%. (Online version in colour.)

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was the loss of power provided by the battery. This issue can be

resolved using a higher capacity battery.

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3. DiscussionThe success rate of directionality control for tethered exper-

iments was higher than that of remote control; 70% versus

60%. Several factors can explain this disparity: first, the added

weight of the electronic backpack and battery will ultimately

cause fatigue in the cockroach and cause it to be less responsive

over time; second, when the roach is allowed to move freely

there is a greater chance for the electrodes to slip out of position;

third, the output signal provided by the system-on-chip will

tend to degrade as the battery loses power; and finally,

human error in control will lead to a reduced reliability. Based

on information from the tethered experiments, improvements

need to be made to the backpack in order to increase reliability

in remote-controlled experiments. The backpack will need to be

lighter, with a more efficient power source to output a consistent

signal for longer periods of time.

During the course of experimentation, it was noted that left

turning in both roach species was much easier to initiate than

the right in both tethered and remote-controlled cases. This

phenomenon further supports our earlier research asserting

that roaches tend to move more frequently toward a left direc-

tion and are thus ‘left-handed’ [11]. It was clear from those tests

that the locomotion of roaches was contralateral to antenna

stimulation, yet turning to one side tended to be easier than

the other, regardless of antenna removal [2,11]. In addition,

the discoid cockroaches will tend to run at a relatively fast

speed when first stimulated. Over time, they tend to walk

more slowly and thus become easier to control. However, the

consistency in response is ultimately based on the skill of

the user controlling the roach. Our experience with these

and prior experiments indicates that adult female discoid cock-

roaches had the highest rate of control. Thus, all tests presented

were conducted using female roaches. Larger roaches were

preferable, as the current backpack system is large. Next gener-

ation systems should be small enough to accommodate smaller

animals, such as the American cockroach. Based on our own

investigation using blank circuit board material, the American

cockroach can best accommodate a 10 mm square circuit

board. The wings and body of American cockroaches are not

as robust as the discoid, and thus cannot support a payload

with a large area. The new system will need to be streamlined

to better conform to the back of the smaller roach. In addition,

adult American cockroaches can comfortably carry 2 g of pay-

load (approx. 10% of body weight) for at least 2 h. In regard to

weight, the limiting factor is the power source. The current

battery weighs 1.5 g, which will need to be changed for next-

generation systems. However, the current battery may be used

if the weight of the circuit board and electronic components

can be drastically reduced. Aside from minimizing the area,

the use of a flexible polymer circuit board material may be ben-

eficial; it will lighten the system and allow it to better conform to

the curvature of the roach’s body.

4. ConclusionA hybrid robotic, remotely controlled cockroach was devel-

oped using precise neural stimulation. Neuron interfacing

and locomotion control was investigated and successfully

implemented in the control of American and discoid cock-

roaches. The effective control responses were observed when

implanting the electrodes inside the area of nerve bundles

of the pro-ganglion (ganglion of the first thoracic segment).

Stimulating this area with electrical pulses elicit movement in

the first set of legs, causing the contralateral leg to become

out of phase with the normal gait of the roach. The application

of a high frequency, low voltage signal to the left or right sides

of the thoracic ganglion of a cockroach will elicit locomotion in

the opposite direction of stimulation. Through the control of

the input signal using a transmitter, a user can control the loco-

motion of the discoid cockroach with high repeatability. The

work presented herein reports advancement in more precise

control of hybrid insects through direct neural stimulation,

and opens new research windows for future development

using these novel approaches.

5. Future workBased on the results obtained during the remote-controlled

trials, it was clear that a feedback control scheme would be

required for more consistency in response of the roach. The cur-

rent system requires visual feedback from the operator in order

to apply the necessary pulse characteristics to control the

roach’s turning behaviour. This method requires the operator

to have extensive experience, as well as constant visual contact

with the roach. However, in a real-world situation the deploy-

ment of a hybrid roach would not be under ideal laboratory

conditions. Therefore, future improvements to our backpack

will include onboard sensors that can relay the locomotion be-

haviour of the roach without having to see its movements.

These sensors may include: on-board compass, accelerometer

and GPS. Our current backpack system is fully capable of inte-

grating these types of sensors. Based on the sensor feedback,

the controller will be programmed to automatically apply the

necessary electrical stimulus to elicit turning in a particular

direction. This will eliminate user error, and make consistency

in response more reliable. Other sensors may also be integrated

into the roach backpack that can relay important information

about the environment such as temperature, humidity and

ambient gases.

6. Material and methods6.1. Insect selectionAdult American and discoid roaches (Periplaneta Americana and

Blaberus discoidalis, respectively) were used in this research. They

were reared in plastic containers kept in a dedicated laboratory,

which was maintained at a constant temperature of 258C and

65% relative humidity, in a 12 h alternating light cycle. The insects

were provided with water, and fed with dog food ad libitum. The

American cockroaches were first studied in order to obtain a

basic knowledge of the required stimulation signals for effective

locomotion control. American cockroaches (length: 32–35 mm;

width: 7–8 mm; mean weight: 6 g) were chosen for this task due

to their high availability and resistance, which allowed for numer-

ous testing trials. Even though they are slow walkers, discoid

cockroaches were later chosen to test the remote control backpack

experiments owing to their larger size (length: 40–43 mm; width:

9–11; mean weight: 7.6 g) which allows for better manipulation of

the on-board electronic system. Besides, these bigger roaches are

also able to carry larger payloads than American cockroaches.

Female roaches are typically larger than male roaches. In addition,

brain

thoracicganglia

abdominalganglia

electrodes

metathoracic ganglion:controls rawmovements of the third pair of legsand hind wings

cercial ganglion: receives informationfrom the cerci and triggers the signalthat initiates the escape reaction

prothoracic ganglion: controls rawmovements of the first pair of legs.Electrodes are inserted into theganglion through the pronotum.mesothoracic ganglion: controlsraw movements of second pair oflegs and forewings

Figure 9. Schematics of neural mapping of discoid cockroaches and responses to stimulation of some ganglia [13,17,18]. (Online version in colour.)

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preliminary experiments showed that female roaches had a higher

rate of control. Thus, only adult female discoid roaches were used

in this study.

6.2. Insect’s neuroanatomy and signal applicationNeuro-anatomical targets were established and simple wire

microelectrodes were used to build a neural interface. The first

set of experiments were conducted using a tethered insect

(American cockroach) in order to obtain stimulation parameters

functioned with sufficient reliability. Previous studies done by

our group using a tethered American cockroach, with amputated

antennae to avoid or diminish other sensory inputs, on a track-

ball system were conducted, showing a detailed description of

the experimental set-up and test results [12]. In summary, Amer-

ican cockroaches were affixed to a stationary platform and made

to run on a trackball system after being neurally stimulated. The

electrodes used in that study were copper and silver wires, and

the output signals were precisely controlled through LabView

software. The trackball experiments aimed to determine the opti-

mum stimulation signal for continual control, as well as monitor

the physical behaviour of the roach over time as it was repeatedly

stimulated. This study gave further insight into the proper place-

ment of electrodes and the optimum stimulation signal for more

accurate turning control of the cockroach. The major finding of

this study showed that the cockroach’s walking and turning be-

haviour can be initiated by asymmetric electrical potential pulses

to the prothoracic ganglion with a success rate of approximately

72%, while previous studies (ours and by other researchers)

using electric pulses through the antennal sockets had success

rates not larger than 50% [6,12]. In this study, a similar approach

was undertaken using free-walking American and discoid cock-

roaches for remote control, but contrary to our previous research,

the antennae of the roaches (American and discoid) were

not amputated. Copper wire electrodes were precisely inser-

ted into the prothoracic ganglion and stimulated using various

electrical signals.

Throughout the course of this study, the general area of

nerves in the ganglia influencing leg movements was identified.

As previously mentioned, ganglia of the three thoracic segments

(pro-, meso- and metathorax) and the bundles of nerves in

contact with leg muscles and wings were studied. This investi-

gation established a map of the various functions responsible

for each segment. Figure 9 schematically illustrates the mapping

of ganglia, nervous cords and nerve bundles in contact with leg

and wing muscles. In general, the nerve bundles located in a par-

ticular thoracic segment are responsible for the control of the pair

of legs from that segment [14,19,20]. When the pulsed patterns of

the electrical signal are sent to the prothoracic ganglion, the loco-

motion command for the first set of legs will be most affected.

The leg located on the side of the stimulation will become out

of phase with the contralateral leg on the same segment, there-

fore, affecting the normal gait of the roach. The stimulated leg

will push more toward the side of the roach, thus causing the

roach to turn in the opposite direction. Figure 10 illustrates

the insertion of electrodes into the prothoracic ganglia of a cock-

roach. The information gained from the study of American

cockroaches was then applied to the larger discoid cockroach,

to implement a remotely operated stimulation system. In this

study, copper electrodes were chosen as they are readily available

and were shown to be electro-chemically responsive to nerve

tissue. Studies have shown that over time, tissue and bodily

ganglia

50 mm

electrodes

(a) (b)

Figure 10. Dissected images of (a) the location of the first thoracic ganglion and (b) placement of two electrodes for localized stimulation in discoid roaches. (Onlineversion in colour.)

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fluids will encapsulate the surface of the electrodes and impede

electron flow [12,16]. However, given the 1-h time frame of the

experiments, the encapsulation will not be severe as to reduce

electrode performance. More effective electrode materials are

currently being investigated.

363

6.3. Hybrid system integrationPrior to the electrode implantation and backpack placement, dis-

coid cockroaches were anaesthetized using carbon dioxide for

10–15 s. Next, a cotton swap soaked in acetone was used to care-

fully remove the thin layer of wax on the pronotum and top

wings [21]. White correction fluid was then used to secure the

wings in place, in preparation for backpack’s attachment. White

correction fluid has been used extensively in this and prior studies

because it is solvent based and not inhibited by the residual wax

coating of the cockroach exoskeleton. In addition, it is easy to

apply, quick drying, and once a test is complete it will flake off

the roach in just a few days. The tip of a 0.35 mm diameter stainless

steel acupuncture needle was then used to puncture two small

holes into the pro-thorax; just above the location of the left and

right side of the prothoracic ganglion. Each hole will receive two

electrodes, a positive and a negative. The electrodes consisted of

0.08 mm, enamel coated, copper wires. Prior to implantation,

two strands of wire glued together using a thin layer of cyanoacry-

late. A small amount of the enamel coating was then removed from

the tips of both wires, ensuring that they did not short the circuit.

The opposite ends of the electrodes were then connected to the RF

circuit board; one wire from each pair connected to a separate

output channel, while the two others were connected to the

common ground.

The circuit board, with electrodes and battery connected, was

then attached to the top surface of the wings using white correc-

tion fluid. A thin piece of wax film (0.5 mm wide, 6 mm long and

thickness , 0.12 mm) was then wrapped over the circuit board

and around the cockroach’s body for more secure attachment.

The wax film was placed in a way that did not affect the natural

walking movements of the cockroach. The two pairs of electrodes

were then carefully placed inside the two puncture holes made

earlier in the pronotum. The electrodes were inserted deep

enough for the exposed region to lie within the central area of

the ganglia on either side. The exact placement of the electrode

pairs was chosen and determined through prior experimentation

and the overall experience of the researcher performing the

implantation [12,16]. Once each electrode pair was placed, a

small drop of white correction fluid was used to secure them

to the cuticle where they entered the cockroach’s body and also

to avoid the roaches losing internal fluids. Figure 1 shows a

discoid cockroach with electronic backpack, battery and electro-

des attached. The entire preparation process took an average of

2 min to complete and was accomplished before the roach was

able to recover from the initial anaesthetization.

For the tethered experiments involving American cockroaches,

a similar preparation process was conducted. In these experiments,

no backpack was placed so there was no need to secure the wings.

Also the tip of a 0.35 mm diameter stainless steel acupuncture

needle was used to puncture two holes into the pronotum above

the left and right portions of the prothoracic ganglia. Similar to

the discoid cockroach’s preparation, two sets of electrodes were

carefully inserted into the holes. The electrodes were prepared

the same way as mentioned above. White correction fluid was

then used to secure the electrodes in place. Since the roaches

were allowed to roam freely in these experiments, a piece of

thread was used to secure them to an overhead fixture. This

allowed the roaches to walk within a specified radius and helped

to prevent the electrodes from being pulled out as they walked.

The thread was affixed to the pronotum using a small drop of

bees wax. The entire preparation process took approximately

2 min to complete and was again achieved before the roach

could fully awaken from the CO2 treatment.

6.4. Radio-controlled stimulation systemThe remote system design is similar to the one designed by UC

Berkeley for experiments involving remote flight control of

beetles [10]. The system-on-chip system was based on the

CC2531 by Texas Instruments. This microcontroller system has

21 general purpose I/O pins and an integrated Zigbee wireless

protocol. For this research, only two I/O pins were used; one

for each stimulation site. Future versions of the system will be

able to use more channels for sensor feedback applications. The

user was able to send right and left turn commands by pressing

buttons located on a transmitter. The receiver on the backpack

then delivered the desired stimulus to the cockroach through

the implanted electrodes. For this research, the output signal

generated by the backpack was set as a þ2.5 V (DC monopolar)

pulse. The duration and the frequency of the pulse were deter-

mined by the length of time in which the button on the

transmitter was depressed. This allowed for optimum control

by the user. Releasing the button would then cease the output

signal. The characteristics of the output signal were determined

through experimentation. As the cockroach moved along the

floor, the user would apply an electrical signal in an attempt to

make it turn left or right. Controlling a free-roaming cockroach

proved to be less predictable than controlling one while tethered.

As such, the stimulation frequency necessary to initiate a turn

with a particular turning radius will vary from roach to roach,

as well as the duration of the test due to the roach becoming fati-

gued. The duration and frequency of stimulation was determined

through visual feedback of the user. For example, if the roach did

not turn with a short signal at a low frequency, a longer signal at

a higher frequency was applied in an attempt to make it turn.

Likewise, if the roach turned at a larger radius than expected,

the stimulation would be adjusted accordingly.

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7. Video of cockroach controlA brief video of a cockroach being remotely controlled can be

seen in electronic supplementary material, video S1. In the

video, a single operator controls the same roach to demon-

strate the robustness of our approach. For purposes of

clarification, two LEDs were added to the electronic backpack

in order to indicate the intended control direction; the green

LED indicates stimulation on the left side of the ganglion

thereby initiating a right turn, likewise the blue LED indicates

stimulation on the right side to initiate a left turn. The video

shows the operator using visual feedback to determine how

and when to stimulate the cockroach to control its locomotion

in a desired direction. The cockroach in the video displayed a

high level of control, at about 65% for the duration of

the trials. Overall, the cockroach was able to be controlled

for 1 h and was given three 5-min rest periods in-between.

Acknowledgements. This work was in part supported by Space andNaval Warfare Systems Command (SPAWAR Grant) No.: N66001-08-1-2063 and Texas A&M University.

Author contributions. C.J.S., C-W.C. and Y.Z. performed the experiments,C.J.S. analysed the data and prepared the first draft. S.B.V. andH. L. supervised the study. C.J.S., S.B.V., J.M.G. and H.L. thoroughlyedited the manuscript. All authors contributed to the interpretationof data. All authors reviewed the manuscript.

oc.Interface

References

12:20141363

1. Brooks RA. 1989 A robot that walks; emergentbehaviors from a carefully evolved network.Neural Comput. 1, 253 – 262. (doi:10.1162/neco.1989.1.2.253)

2. Delcomyn F. 1999 Walking robots and the centraland peripheral control of locomotion in insects.Auton. Robots 7, 259 – 270. (doi:10.1023/A:1008928605612)

3. Raibert MH. 1986 Legged robots. Commun. ACM 29,499 – 514. (doi:10.1145/5948.5950)

4. Melzack R, Wall PD. 1965 Pain mechanisms: a newtheory. Science 150, 971 – 979. (doi:10.1126/science.150.3699.971)

5. Shealey CN, Mortimer JT, Reswick JB. 1967 Electricalinhibition of pain by stimulation of the dorsalcolumns: preliminary clinical report. Anesth. Analg.46, 489 – 491.

6. Holzer R, Shimoyama I. 1997 Locomotion control ofa bio-robotic system via electric stimulation. Proc.Int. Conf. Intell. Robots Syst. 3, 1514 – 1519.

7. Carlo M, Metin S. 2006 A biomimetic climbing robotbased on the gecko. J. Bionic Eng. 3, 115 – 125.(doi:10.1016/S1672-6529(06)60015-2)

8. Mika B, Lee H, Gonzalez JM, Vinson SB, Liang H.2007 Studying insect motion with piezoelectricsensors. Proc. SPIE 6528, 1 – 10. (doi:10.1117/12.715885)

9. Lee H, Cooper R, Mika B, Clayton D, Garg R,Gonzalez JM, Vinson SB, Khatri S, Liang H. 2007

Polymeric sensors to monitor cockroach locomotion.IEEE Sens. J. 7, 1689 – 1702. (doi:10.1109/JSEN.2007.909624)

10. Hirotaka Sato CWB, Peeri Y, Baghoomian E,Casey BE, Lavella G, VandenBrooks JM,Harrison JF, Maharbiz MM. 2009 Remoteradio control of insect flight. Front. Integr.Neurosci. 3, 24.

11. Cooper R, Nudo N, Gonzalez J, Vinson SB, Liang H.2011 Side-dominance of Periplaneta americanapersists through antenna amputation. J. InsectBehav. 24, 175 – 185. [English] (doi:10.1007/s10905-010-9246-4)

12. Chiu CW, Sanchez C, Zhou Y, Gonzalez JM, HarlowM, Vinson SB, Liang H. 2012 In vivo neuralstimulation for locomotion control of cockroaches.Trends Entomol. 8, 66 – 73.

13. Bozkurt A, Gilmour RF, Lal A. 2009 Balloon-assistedflight of radio-controlled insect biobots. IEEE Trans.Biomed. Eng. 56, 2304 – 2307. (doi:10.1109/TBME.2009.2022551)

14. Mu L, Ritzmann R. 2005 Kinematics and motoractivity during tethered walking and turning in thecockroach, Blaberus discoidalis. J. Comp. Physiol. A191, 1037 – 1054. [English] (doi:10.1007/s00359-005-0029-x)

15. Latif T, Bozkurt A. (eds). 2012 Line followingterrestrial insect biobots. In 2012 Annual Int. Conf.of the IEEE on Engineering in Medicine and Biology

Society (EMBC), 28 August 2012 – 1 September2012, San Diego, CA.

16. Chiu C-W, Gonzalez JM, Harlow M, Vinson BS,Liang H. 2012 Electrode – immune system interfacemonitor through neural stimulation in Americancockroach (Periplaneta americana). Electrochim.Acta 68, 81 – 87. (doi:10.1016/j.electacta.2012.02.046)

17. Harris JT, Eisenstein EM. 1999 Transfer of learnedinformation between ganglia in the insect ventralnerve cord. Behav. Brain Res. 103, 211 – 217.(doi:10.1016/S0166-4328(99)00039-X)

18. Eisenstein EM, Reep RL, Lovell KL. 1985 Avoidanceand escape components of leg position learning inthe prothoracic and mesothoracic ganglia of thecockroach, P. americana. Physiol. Behav. 34,129 – 132. (doi:10.1016/0031-9384(85)90090-3)

19. Reep RL, Eisenstein EM, Tweedle CD. 1980 Neuronalpathways involved in transfer of information relatedto leg position learning in the cockroach,P. americana. Physiol. Behav. 24, 501 – 513. (doi:10.1016/0031-9384(80)90244-9)

20. Camhi JM. 1980 The escape system of thecockroach. Sci. Am. 243, 158 – 172. (doi:10.1038/scientificamerican1280-158)

21. Cooper R, Lee H, Gonzalez JM, Butler J, Vinson SB,Liang H. 2009 Lubrication and surface properties ofroach cuticle. J. Tribol. 131, 014 502 – 014 504.(doi:10.1115/1.3002327)