www.sciencemag.org/content/350/6258/314/suppl/DC1
Supplementary Materials for
A skin-inspired organic digital mechanoreceptor
Benjamin C.-K. Tee, Alex Chortos, Andre Berndt, Amanda Kim Nguyen, Ariane Tom, Allister McGuire, Ziliang Carter Lin, Kevin Tien, Won-Gyu Bae, Huiliang Wang, Ping Mei,
Ho-Hsiu Chou, Bianxiao Cui, Karl Deisseroth, Tse Nga Ng, Zhenan Bao* *Corresponding author. E-mail: [email protected]
Published 16 October 2015, Science 350, 314 (2015) DOI: 10.1126/science.aaa9306
This PDF file includes: Materials and Methods
Figs. S1 to S14
Tables S1 and S2
Caption for movie S1
References
Other supplementary material for this manuscript includes the following: Movie S1
2
Materials and Methods
Ring oscillator fabrication and testing
The organic field-effect transistors are in top-gate geometry and are fabricated on plastic
polyethylene naphthalate foils as described in Refs (15, 16). The electrodes are inkjet printed using
Ag nanoparticle dispersion from Colloidal Ink in Japan. Organic semiconductors from Flexink and
Polyera were inkjet printed to form p-channel and n-channel transistors. The gate dielectric is a
bilayer, comprised of a Teflon layer (from Dupont) next to the semiconducting layer and a high-k
PVDF-TrFE-CTFE relaxor polymer (from Piezotech). All fabrication and measurement are done
in air. We tested the ring oscillator using an active probe and low-input capacitance unity gain
buffer, which was used for interfacing a conventional silicon edge-detector chip with the organic
circuits For optical neuron stimulation, an edge detector circuit was added to obtain a pulse width
of 2 ms. With continuous stimulation, the neurons fire at their natural frequency (~300 Hz).
Consequently, the pulse width must be smaller than the inverse of this frequency (3.3 ms) to avoid
producing multiple action potentials with one oscillation of the oscillator. Therefore, the edge
detector was necessary to ensure the desired property of producing one action potential per
oscillation of the sensor. The complete circuit diagram is included as Fig. S14. The buffer and edge
detector circuits are conventional silicon chips, but in future versions, it could be straightforward
to eliminate the buffer and monolithically integrate the oscillator and edge detector on one substrate
to have a fully printed organic digital e-skin.
Piezoresistive sensor fabrication
Single-walled carbon nanotubes (CNTs) were obtained from Carbon Solutions, Inc. (P2-SWNT).
10 mg of CNTs were dispersed in NMP by sonicating for 30 minutes using a tip horn sonicator
(Cole Parmer ultrasonic processor 750 W) at 30% power. The resulting solution was centrifuged
at 8000 RPM for 30 minutes using a Sorvall Lynx 4000 centrifuge. The solution was spraycoated
onto a silicon wafer at 200°C to form a conducting electrode. A solution of polyurethane
elastomer (SG80A from Lubrizol) was spincoated onto the electrode. The electrode was
subsequently transferred onto a polyurethane substrate. To form the piezoresistive composite, 20
mg of CNTs in 9 mL of chloroform were dispersed by sonicating for 20 minutes at 30% power.
After adding 1 mL of a 10 mg/mL solution of poly-3-hexylthiophene (Sepiolid P100), the
solution was sonicated for another 60 minutes, and was subsequently centrifuged for 20 minutes
at 6000 RPM. The dispersed CNTs were mixed with a solution of polyurethane (SG80A from
Lubrizol) in chloroform and spincoated onto PDMS molds of pyramid structures. The CNT
electrodes were laminated on top of the piezoresistive pyramids and heated at 60°C for 5 minutes
to ensure good bonding. The CNT electrode/piezoresistive composite stack was then removed
from the mold. As the counter electrodes, we used evaporated gold on glass slides as rigid
electrodes or spraycoated silver nanowires (AW060 from Zhejiang Kechuang Advanced
Materials Technology Co., Ltd.) embedded in PDMS as stretchable electrodes.
Mutagenesis of iC1C2(s/v) and testing in cultured neurons
DNA sequence of n-terminal modified C1C2 version bC1C2 was synthesized (Genescript) and
cloned into AAV vectors containing the CamKIIα promoter for expression in neurons. The
construct was fused to eYFP DNA (enhanced yellow fluorescent protein) to detect protein
expression in neurons by fluorescence microscopy. Mutations (I170V and Q95S) were introduced
using QuickChangeTM Site-Directed mutagenesis kit (Agilent). Plasmid DNA was purified with
QIAprepTM Spin Miniprep Kits (Qiagen) after transformation and amplification in E. coli.
3
Electrophysiological recordings in neuronal cultures were prepared as described(27). Patch pipettes
(4-6 MΩ) were pulled from glass capillaries (Sutter Instruments) with a horizontal puller (P-2000,
Sutter Instruments) for whole-cell recordings in voltage and current clamp. Recordings were made
using a MultiClamp700B amplifier (Molecular Devices). The external recording solution contained
(in mM): 127 NaCl, 10 KCl, 10 HEPES, 2 CaCl2, 2 MgCl2, 30 D-glucose, pH 7.3, including
synaptic blockers (25 µM D-APV, 10 µM NBQX). The patch pipette solution contained (in mM):
140 K-gluconate, 10 HEPES, 10 EGTA, 2 MgCl2, pH 7.3. Series resistance was monitored
throughout recordings for stability. A Spectra X Light engine (Lumencor) was used to excite eYFP
and to apply light for opsin activation. Stimulation light (475 nm) was applied through a 40X
objective (Olympus) at 5 mW/mm2 light intensity. Photocurrents were measured at -80 mV in
voltage clamp mode during 1 s light application. All reported values refer to the stationary
photocurrents. The activation spectra for bC1C2(s/v) and ChR2(HR) were measured by recording
stationary photocurrent in voltage clamp mode at -80 mV and light intensities of 0.65 mW/mm2 at
each wavelength. Light was delivered through 20 nm bandbass filters (Thorlabs) at (in nm): 400,
420, 440, 460, 480, 500, 520, 540, 560, 580, 600. Photocurrents were normalized to 480 nm.
Kinetics of channel closure were determined by fitting the decay of photocurrents after light-off,
with mono-exponential or bi-exponential functions. Channel kinetics were quantified by
corresponding tauoff values respectively. pClamp10.3 (Molecular Devices) and OriginLab8
(OriginLab) software was used to record and analyze data.
Stereotactic virus injection
The following adeno-associated viruses (AAV) with serotype DJ were produced at the Stanford
Neuroscience Gene Vector and Virus Core: double floxed AAVdj-EF1a-DIO::ChR2(E123A)-
EYFP and AAVdj-EF1a-DIO::bC1C2(s/v)-EYFP 4-6 week old PV+-IRES-Cre mice were injected
bilaterally with 1 µl of either virus in the medial prefrontal cortex (mPFC) or the primary
somatsensory cortex forelimb region (S1FL), at the following coordinates (from bregma): AP +1.7
mm, ML +0.3 mm, DV -2.5 mm (mPFC) or AP +0.26 mm, ML +2.1 mm, DV -1.5 mm (S1FL).
Titer were matched at 1.5x1012 vg/ml for both viruses. Expression is controlled by Cre-recombinase
and restricted to parvalbumin positive cells (PV+). Expression is controlled by Cre-recombinase
and restricted to parvalbumin positive cells (PV+).
Acute slice electrophysiology
Acute brain slices were prepared from mouse medial prefrontal cortex (mPFC) or primary
somatsensory cortex forelimb region (S1FL) 4-6 weeks after viral injection. Coronal slices (300
μm) from injected mice were prepared after intracardial perfusion with ice-cold, sucrose-containing
artificial cerebrospinal fluid solution (ACSF; in mM): 85 NaCl, 75 sucrose, 2.5 KCl, 25 glucose,
1.25 NaH2PO4, 4 MgCl2, 0.5 CaCl2 and 24 NaHCO3. Slices recovered for 1 hour at 32–34 °C, and
then were transferred to an oxygenated recording ACSF solution (in mM): 123 NaCl, 3 KCl, 26
NaHCO3, 2 CaCl2, 1 MgCl2, 1.25 NaH2PO4 and 11 glucose, at room temperature.
Electrophysiological recordings were performed at 32–34 °C under constant perfusion of the
oxygenated recording ACSF solution. For mPFC recordings, synaptic transmission blockers (D-2-
amino-5-phosphonovaleric acid (APV; 25 μM), 2,3-dihydroxy-6-nitro-7-sulfamoyl-
benzo[f]quinoxaline-2,3-dione (NBQX; 10 μM) and gabazine (10 μM)) were added to the
recording ACSF solution. Slices were visualized with an upright microscope (BX61WI, Olympus)
under infrared differential interference contrast (IR-DIC) optics. A Spectra X Light engine
(Lumencor) was used both for viewing fluorescent protein expression and delivering light pulses
for opsin activation. PV+ neurons were identified by eYFP+ expression. Whole-cell voltage-clamp
recordings were performed at -80 mV, and current-clamp recordings were performed at rest. Patch-
clamp pipettes contained the following internal solution (in mM): 125 K-gluconate, 10 KCl, 10
HEPES, 4 Mg3-ATP, 0.3 Na-GTP, 10 phosphocreatine, 1 EGTA. Recordings were conducted using
MultiClamp700B amplifier and pClamp10.3 software (Molecular Devices). pClamp10.3,
4
OriginLab8 (OriginLab), and SigmaPlot (SPSS) were used to analyze data. Stationary photocurrent
of the opsins was measured at the end of a 1-s light pulse (475 nm) in voltage-clamp mode. Light-
evoked spike probability in the PV+ neurons was calculated as the fraction of successful action
potentials evoked in neurons at light stimulation frequencies ranging from 40 to 200 Hz during a 4
second stimulation period.
Electrical neuron stimulation with inorganic oscillators
Prior to cell plating, multi-electrode arrays (MEAs) were cleaned with a brief oxygen plasma and
coated with 200 μg/mL poly-L-lysine. Hippocampal [or cortical] neurons were isolated from E18
rats and cultured for 10-14 days on MEAs as previously described. The neurons were maintained
in neurobasal medium supplemented with B27, penicillin/streptomycin, and L-glutamine.
Electrical activity of primary neuron cultures was stimulated by an external stimulation
macroelectrode (to achieve spatial control) and recorded by planar (Multi-electrode arrays) MEAs.
The stimulating macroelectrode was connected to a pulse generator, which was in turn connected
to the DiTact sensor. Commercial signal processing and amplification were used (Multichannel
Systems) to record both stimuli and evoked cellular responses.
5
DiTact sensor characterization
Fig. S1. Images of organic ring oscillators. (A) Array of printed complementary ring oscillators.
Zoomed-in area shows the 3-stage ring oscillator. Each oscillator pixel is composed of three
inverters that form the oscillator and one additional inverter that functions as a buffer. The
oscillators near the top of the substrate are five stage oscillators and the ones near the bottom of the
substrate are three-stage oscillators (B) Voltage output of a three-stage ring oscillator showing a
frequency of 110 Hz at a supply voltage of 8V.
6
Fig. S2. Electrical characteristics of p- and n-type transistors in the complementary organic
oscillators. (A) Transfer curves and (B) output curves for p-type devices. P-type devices had a W/L
of 42 and a mobility of 0.10 cm2V-1s-1. (C) Transfer curves and (D) output curves for n-type devices.
N-type devices had a W/L of 60 and a mobility of 0.07 cm2V-1s-1.
7
Pressure Sensor Characterization
Fig. S3. Effect of pyramid size on the pressure response of piezoresistive sensors. Small
pyramids (3 μm) have higher sensitivity, but smaller dynamic range. 50 μm pyramids have the
desired sensing properties throughout the pressure range of interest. The voltage was 5 V.
8
Fig. S4. Effect of pyramid spacing on the pressure response of the piezoresistive sensors. As
the spacing between pyramids increases, the sensitivity increases. However, when pyramids are
spaced far apart, the region between the pyramids comes in contact with the substrate, preventing
recovery to the initial impedance. The pressure at which device characteristics become
irrecoverable decreases as pyramid spacing increases. With a spacing of 50 μm, the device
properties are recoverable throughout the measurement range. With a spacing of 100 μm,
irrecoverable deformation occurs at ~40 kPa, and with a spacing of 200 μm, irrecoverable
deformation occurs at only 20 kPa. The voltage was 5 V.
10
Figure S4. Effect of pyramid spacing on the pressure response of the piezoresistive sensors. As the
spacing between pyramids increases, the sensitivity increases. However, when pyramids are spaced
far apart, the region between the pyramids comes in contact with the substrate, preventing recovery
to the initial impedance. The pressure at which device characteristics become irrecoverable
decreases as pyramid spacing increases. With a spacing of 50 μm, the device properties are
recoverable throughout the measurement range. With a spacing of 100 μm, irrecoverable
deformation occurs at ~40 kPa, and with a spacing of 200 μm, irrecoverable deformation occurs at
only 20 kPa. The voltage was 5 V.
9
Fig. S5. Voltage dependence of the sensor impedance. The voltage dependence can be
approximated as exponential (R2 > 0.98).
Data Fitting for Sensor Pressure Dependence
The sensors function partially based on changes in the tunneling barrier as a function of
pressure. Tunneling current density is substantially influenced by the applied voltage.
Consequently, the pressure sensor characteristics are voltage-dependent. This is important for the
DiTact sensor because in a voltage divider configuration, the voltage across the piezoresistor
changes with applied pressure, resulting in a complex relationship between the pressure and voltage
dependence. Fig. S6 depicts the voltage dependence and fitted characteristics of a model sensor.
10
Fig. S6: Experimental and fitted sensor impedance. (A) Dependence of the impedance of the
sensor on the pressure and voltage. (B) Fitted value of the impedance as a function of pressure and
voltage. The fitting process gave an R2 value of 0.975. (C) The log value of the residuals from the
fitting process.
The magnitude of the impedance can be modeled using equation (1), where Zsensor is the
impedance of the sensor, P is the pressure, Vsensor is the voltage across the sensor, and a1 to a5 are
parameters to be fit to the data. The electric field dependence of tunneling currents from CNT
electrodes can often be approximated by an exponential fit(28, 29). The impedance of a
piezoresistive sensor based on tunneling depends exponentially on the applied strain(30).
Consequently, the pressure dependence is determined by the stress-strain behavior of the device.
11
The deviation from exponential behavior caused by the shape of the pyramids is taken into account
by the exponent on the pressure term (a4).
𝑍𝑠𝑒𝑛𝑠𝑜𝑟 = 𝑎110^(𝑎2𝑉𝑠𝑒𝑛𝑠𝑜𝑟 + 𝑎3𝑃𝑎4) (1)
The circuit diagram for the sensing element is show in Fig. S7. The reference resistor is not
necessary in the device, but can be useful for tuning the pressure response characteristics (Fig. S9).
Therefore, in addition to the piezoresistive composite composition and the structure of the pyramids
in the piezoresistive sensor, the reference resistor adds another method of modifying the device
output. Tunable characteristics are important because mechanoreceptors in different parts of the
body have different saturation frequencies, different sensitivities, and different shapes of the
frequency vs stimulus curves(18).
Equation (2) provides the voltage across the oscillator which is the supply voltage of the
oscillator. The fitted equation for the impedance of the sensor (1) can be substituted into the
equation for the voltage across the oscillator (2), resulting in a non-linear implicit equation for the
dependence of Vosc on the applied pressure. Furthermore, as shown in Fig. 1c, the impedance
through the oscillator is also voltage-dependent. The resulting equation was solved using MATLAB
to determine the voltage across the sensor and the oscillator for each pressure value. The pressure
and the voltage across the sensor and the impedance of the sensor for the fitted data from Fig. 2c
are plotted in Fig. S8.
𝑉𝑜𝑠𝑐 =[𝑍𝑜𝑠𝑐
−1 +𝑍𝑟𝑒𝑠𝑖𝑠𝑡𝑜𝑟−1 ]
−1
[𝑍𝑜𝑠𝑐−1 +𝑍𝑟𝑒𝑠𝑖𝑠𝑡𝑜𝑟
−1 ]−1
+ 𝑍𝑠𝑒𝑛𝑠𝑜𝑟𝑉𝑎𝑝𝑝𝑙𝑖𝑒𝑑 (2)
12
Fig. S7. Circuit diagram used for calculating pressure dependence. The voltage dependence of
the pressure sensor characteristics as well as the voltage dependence of the oscillator impedance
must be taken into account to accurately predict the frequency of the sensor.
13
Fig. S8. Sensor voltage fit during pressure test. Fitted values of the impedance of the pressure
sensor and the voltage across the sensor as a function of pressure for the circuit shown in fig. S7
without a resistor (resistor with infinite impedance).
The modeled electrical properties of the circuit was used to investigate some aspects of the circuit’s
response to pressure. Fig. S6 shows the effect of different reference resistor values on the pressure
dependence of the sensing characteristics.
14
Fig. S9: Effect of reference resistors on frequency output. As the impedance of the reference
resistor decreases, the sensitivity decreases while the working range increases. Furthermore, the
shape of the curve becomes more linear.
15
Channelrhodopsin Protein Characterization
We replaced the first 49 amino acids by the first 11 amino acids of ChR2 to improve membrane
trafficking and expression. As shown before, introduction of the mutation I131V accelerated
channel closure(31), which we further enhanced by replacing glutamine 56 by serine (Q56S).
Fig. S10. bC1C2(v/s) characterization in cultured neurons. (A) Schematic composition of
channelrhodopsin hybrids C1C2 and bC1C2(v/s): Both contain segments from channelrhodopsin 1
and 2 (ChR1 and 2). Numbers indicate amino acid positions. bC1C2(s/v) was mutated at positions
56 (Q56S) and 131 (I131V) to accelerate channel kinetics. The first 39 amino acids were replaced
by the first 11 amino acids of ChR2 to improve expression and membrane trafficking. (B)
Activation spectrum of bC1C2(v/s) (red) compared to ChR2(HR) (black). Each construct n = 3. All
error bars indicate s.e.m., n indicates number of cells. (C) Photocurrents amplitudes -80 mV: ChR2-
H134R (ChR2(HR), n = 24), ChR2-E123A (ChETA(EA), n = 18), C1C2 (n = 18), bC1C2(IV)
(bC1C2(I131V), n = 15) and bC1C2(s/v) (n = 19). (D) Left: tau-values of mono-exponential off-
kinetics (ChR2(HR), ChETA(EA), C1C2) and the fast components of bi-exponential off-kinetics
(C1C2(IV), bC1C2(s/v)). Same n as in (A). Right: Proportion of photocurrent amplitudes decaying
with fast tau-off.
16
17
Fig. S11. Comparison of fast channelrhodopsin bC1C2(v/s) and ChETA(EA) (A) Decay of
photocurrents after 475 nm light excitation (blue bar). Current traces were normalized to compare
speed of channel closures. bC1C2(s/v) (red) off-kinetics are bi-exponential with a fast and slow
component. ChETA(EA) (black) current decays exponentially. (B) Photocurrent amplitudes
measured in cortical parvalbumin positive (PV+), fast spiking interneurons of mice medial
prefrontal cortex (mPFC). ChETA(EA): n = 16, bC1C2(s/v): n = 10. (C) Left: tau-values of mono-
exponential ChETA(EA) off-kinetics and the fast bi-exponential bC1C2(s/v) off-kinetics.
ChETA(EA): n = 16, bC1C2(s/v): n = 10. Right: Proportion of photocurrent amplitudes decaying
with fast and slow tau-off.
18
Fig. S12. Comparison of real and artificial mechanoreceptors. (A) Pressure response of
biological mechanoreceptors in the human foot.(32) Reproduced with permission. (B) Frequency
of action potentials vs pressure for parvalbumin interneurons in the prefrontal cortex coupled to the
DiTact sensor. There is a good correlation in the threshold frequency and maximum frequency. The
first three trials depicted were from different locations on a sample with a CNT content of 1.17
wt%. The fourth trial was conducted using a sensor with a smaller concentration of CNTs and
shows a lower sensitivity. The operation voltage was 8 V, resulting in a max frequency of 130 Hz
and a max power consumption of 4.5 µW. (C) Indentation response of biological mechanoreceptors
in the human fingertip.(33) Reproduced with permission. (D) Frequency of action potentials vs
pressure for neurons in the primary somatosensory cortex coupled to the DiTact sensor. All ten
trials used the same oscillator and sensor. The operation voltage was 11 V, resulting in a max
19
frequency of 200 Hz and a max power consumption of 18.4 µW.
Fig. S13. Electrical stimulation of plated hippocampal neurons.. (A) A ramped pressure from 0
to 100kPa was applied. The stimulation pulse frequency increases proportionally with the pressure
with the neuron firing tracking the stimulation frequency. (B) Three instance of stimulated neuron
firing from tactile sensor. (C) Panel shows a single action potential triggered from a stimulation
pulse due to pressure. An inorganic oscillator was used as the source of oscillation.
20
Fig. S14: Full circuit diagram of the elements used for interfacing the DiTact sensor with the neuron
stimulation equipment. The buffer is a unity gain low-input capacitance node for interfacing
conventional silicon edge-detector chip with organic circuits.
21
Photocurrents
(pA)
± s.e.m / n
tauoff
(ms)
± s.e.m /
n
fast tauoff
(ms)
± s.e.m / n
slow tauoff
(ms)
± s.e.m
% of
photocurrent
w/ fast tauoff
± s.e.m
% of
photocurrent
w/ slow tauoff
± s.e.m
ChR(HR) 868.8
± 79.4 / 24
38.8
± 8.7 / 24
- - - -
ChETA(EA) 657.9
± 72.0 / 18
18.8
± 1.3 / 18
- - - -
C1C2 1212.9
± 129.9 / 18
30.7
± 1.0 / 18
- - - -
bC1C2(IV) 1284.5
± 98.7 / 15
- 14.7
± 0.81 / 15
137.8
± 14.9
88.2
± 0.1
11.8
± 0.1
bC1C2(s/v) 1245.8
± 118.87 / 19
- 8.9
± 0.55 / 19
129.7
± 20.8
87.0
± 0.1
13.0
± 0.1
Supp. Table 1. Biophysical properties of channelrhodopsin variants in cultured neurons of
mouse hippocampus. s.e.m. is standard error of the mean. n indicates number of cells
22
Photocurrents
(pA)
± s.e.m / n
tauoff
(ms)
± s.e.m / n
fast tauoff
(ms)
± s.e.m / n
slow
tauoff
(ms)
± s.e.m
% of
photocurrent
w/ fast tauoff
± s.e.m
% of
photocurrent
w/ slow tauoff
± s.e.m
ChETA(EA) 311.1
± 50.2 / 16
7.0
± 0.3 / 16
- - - -
bC1C2(s/v) 704.1
± 101.1 / 10
- 3.4
± 0.2 / 10
31.2
± 2.0
78.6
± 1.6
21.4
± 1.6
Supp. Table 2. Biophysical properties of ChETA(EA) and bC1C2(s/v) in cultured neurons
of mouse hippocampus. s.e.m. is standard error of the mean. n indicates number of cells.
23
Movie S1
The movie shows the flexible DiTact sensors mounted on a wearable glove. At zero pressure stimuli, the sensor outputs no digital signal. The glove was used to apply pressure on a digital weighing scale. The output from the monitor shows the frequency output from the DiTact sensors. As the pressure increases, the frequency increase.
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SOM.page.1.EXPRESS.no.movies.pdfA skin-inspired organic digital mechanoreceptor
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