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 SPIEDigitalLibrary.org/conference-proceedings-of-spie

 Field-effect electro-plasmonics: a
 quantum leap in neurotechnologies

 Habib, Ahsan, Zhu, Xiangchao, Can, Uryan, McLanahan,
 Maverick, Zorlutuna, Pinar, et al.

 Ahsan Habib, Xiangchao Zhu, Uryan I. Can, Maverick McLanahan, Pinar
 Zorlutuna, Ahmet Ali Yanik, "Field-effect electro-plasmonics: a quantum leap
 in neurotechnologies," Proc. SPIE 11461, Active Photonic Platforms XII,
 1146129 (4 September 2020); doi: 10.1117/12.2569154

 Event: SPIE Nanoscience + Engineering, 2020, Online Only

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Invited Paper

 Field-Effect Electro-Plasmonics:
 A Quantum Leap in Neurotechnologies
 Ahsan Habiba, Xiangchao Zhua, Uryan I. Canb, Maverick L. McLanahanc, Pinar Zorlutunad,
 Ahmet Ali Yanika*
 a
 Baskin School of Engineering, University of California Santa Cruz, Santa Cruz, CA, 95064, USA;
 d
 Aerospace and Mechanical Engineering, University of Notre Dame, Notre Dame, IN, 46556, USA;
 c
 Physics Department, University of California Santa Cruz, Santa Cruz, CA, 95064, USA.
 Correspondence to: Email: yanik@ ucsc.edu

 ABSTRACT

 State-of-art electro-optic translators cannot provide high signal-to-noise ratio electric-field measurement capability due to
 whether low photon counts (e.g., voltage sensitive dyes) or low electric-field sensitivities (e.g., quantum dots). Here, we
 demonstrate that electrochromic loading of plasmonic (electro-plasmonic) nanoantenna allows us to overcome these
 limitations and to realize extremely bright, sensitive and fast nanoscale electric-field probes. Our electro-plasmonic
 nanoantennas have 10-100 million times larger cross sections than fluorescence dye molecules and provide three orders of
 magnitude enhanced electric-field sensitivities than conventional plasmonic nanoantennas with sub-millisecond temporal
 response times (~ 0.2 ms). In our experiments, we demonstrated label-free optical detection of electrogenic activity of stem
 cell derived cardiomyocytes with high signal-to-noise ratios at low light intensity conditions. Our novel approach presents
 a remarkable technological leap for label-free optical imaging of electric-field dynamics with high spatiotemporal
 resolution.
 Keywords: Active plasmonics, electro-plasmonics, nanoantenna, neurophotonics, label-free detection, electrophysiology.

 1. INTRODUCTION
 Plasmonic nanoantenna can dramatically concentrate light (down to105 times smaller volumes than the diffraction limited
 volume) and offer an abundance of exciting opportunities for biomedical applications [1-10]. Strongly enhanced near-
 fields of localized surface plasmons (LSPs) allow transduction of small fluctuations in the local refractive index to easily
 detectable spectral signals in the far-field spectra [2, 11-15]. Label-free biosensing technologies based on these concepts
 are well established; down to a single molecule detection capabilities are shown [16-18]. However, there is very limited
 progress towards real-time optical detection of local electrical field dynamics, which is highly desirable for the detection
 of the extracellular electrophysiological signals. During the past decade, there has been a concentrated effort to develop
 active plasmonic devices using inherent voltage sensitivity of noble metals for local field measurements. However, due to
 the high electron densities, the inherent voltage sensitivities of the metals are low. Electro-optic effects in metals are
 extremely weak [19].
 Here we are presenting a new class of extremely bright non-fluorescent optical voltage sensors that can sensitively detect
 local electric-field dynamics. With more than 3.25´103 times enhanced field sensitivities over conventional plasmonic
 nanoantennas, our electrochromically loaded plasmonic (electro-plasmonic) nanoantennas enable high signal-to-shot-noise
 ratio (SSNR~40-250) local electric field measurements with light in a label-free fashion. Our electro-plasmonic probes
 compare demonstrate superior characteristics with respect to the state-of-the-art optical probes, such as genetically encoded
 voltage indicators (GEVIs), which have a low SSNR [20-22] due to small cross-sections (~10−2 nm2) [23] and low quantum
 yields (~10−3 to 10−2)[24]. Furthermore, we have demonstrated a label-free and non-invasive optical measurement of the
 electrogenic activity of cardiac muscle cell (CM) through our in vitro measurements using low-intensity light, which is
 two to three orders of magnitude lower than the typical light intensities used for GEVIs [22].

 Active Photonic Platforms XII, edited by Ganapathi S. Subramania, Stavroula Foteinopoulou, Proc. of SPIE
 Vol. 11461, 1146129 · © 2020 SPIE · CCC code: 0277-786X/20/$21 · doi: 10.1117/12.2569154

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2. MATERIALS AND METHODS
 Electron beam lithography (EBL) was used to fabricate the plasmonic nanoantenna array (Fig.1a). A positive photoresist,
 495 PMMA A4 (Microchem, USA), was spin coated (4000 rpm) on the ITO glass slides (Structure probe, Inc., US A) and
 then baked at 180° C on a hot plate for 90 seconds. The nanometer pattern generation system (NPGS) was used for electron
 beam patterning (90 nm in diameter gold nanoantennas with a periodicity of 500 nm) with an FEI Quanta 3D field emission
 microscope. Subsequently, the sample was developed for 1 minute in isobutyl ketone (MIBK)-isopropanol (IPA) solution
 (MIBK: IPA=1:3) (Microchem, USA) and was placed in an IPA solution for 1 minute to stop the development. The sample
 was then dried under a stream of high-purity nitrogen. A 45 nm thick gold layer (Kurt J. Lesker, USA) electron beam
 evaporation process was performed. Deposition was done at 1.2 x 10-6 pressure and 0.5 Å/sec evaporation rate. The sample
 was dipped into acetone and subsequently a brief (~5 s) metal liftoff process was performed with ultrasonication.

 Figure 1. Electro-plasmonic nanoantenna fabrication and characterization. (a) Fabrication steps of the electric field probe using electron
 beam lithography (EBL) and electrochemical deposition. (b) Scanning electron microscope (SEM) image of the electro-plasmonic field
 probe.

 PEDOT: PSS was selectively deposited on nanoantenna in a monomer of 10 mM EDOT (Sigma-Aldrich, USA) and 0.1M
 NaPSS (Sigma-Aldrich, USA) into an aqueous solvent using a custom developed electrochemical deposition technique.
 The deposition was carried out in a three-electrode electrochemical cell under the potentiostatic conditions: the working
 electrode was the nanoantenna array, the counter-electrode was the platinum coil (Alfa Aesar, USA) and the reference
 electrode was Ag/AgCl (Warner instruments, USA). The electro-plasmonic nanoantenna consisted of PEDOT: PSS layer
 as shown in Figure 1b. In the final step, neonatal rat ventricular cardiac muscle cell (CM) was seeded on the electro-
 plasmonic nanoantenna according to a previously established protocol [25].

 3. RESULTS AND DISCUSSION
 We performed electro-optic measurements to determine the field sensitivity of our device within an external 10-2-10-3
 mV/nm electric field range, which is comparable to extracellular fields [26]. Figure 2a illustrates the optical setup used.
 The measurement was performed with controlled electric fields generated through a transparent counter electrode.

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Figure 2. Electro-optic characterization of electro-plasmonic field probe. (a) Scanning electron microscope (SEM) image of the electro-
 plasmonic field probe. (b) Electric field sensitivity of the electro-plasmonic nanoantenna.

 We have developed a quasi-static model that treats Au particles and conducting polymer as Drude metals to provide a
 physical insight into linear dependence of the signal to the external electric field. The spectral modulation due to dielectric
 constant variations in the electrochromic PEDOT: PSS load can be expressed as in [7]:

 ⎡ ⎤
 ⎢ ⎥
 Δλ LSP
 ω λ ⎢
 2 3
 (1− L ) L ⎥
 = 2 Δε PEDOT
 EP p LSP
 (1)
 8π c ⎢ ⎛
 2 2
 ⎛ 1− L ⎞ ⎞ ⎥
 ⎢ ⎜ ε ∞ + ε PEDOT ⎜ ⎥
 ⎢⎣ ⎝ ⎝ L ⎟⎠ ⎟⎠ ⎥⎦

 where L is the geometrical factor for the nanoantenna, ω p is the metal plasma frequency, ε ∞ is the high frequency
 contribution to metal dielectric function, and ePEDOT is the dielectric constant of the PEDOT film. Here, the resonance
 wavelength shift Δλ LSP is linearly proportional to the DePEDOT, the change in the PEDOT: PSS load permittivity with
 EP

 electric field. Following Drude model [27, 28], DePEDOT can be expressed as [7]:
 ω 3p,PEDOT ⎛ ε0 ⎞
 Δε PEDOT =− 2 2 ⎜ PEDOT ⎟
 E (2)
 γ PEDOT + ω ⎝ N PEDOT edTF ⎠

 where dTFPEDOT = 1/ 2(ao3 / N PEDOT )1/6 is the Thomas-Fermi screening length, ao = 5.29 × 10−11 m is the Bohr radius, NPEDOT is
 the free electron density in PEDOT conducting polymer. wp,PEDOT is the bulk plasma frequency, e¥,PEDOT is the relative
 permittivity at the high-frequency limit and gPEDOT is the damping coefficient, e is the electron charge, and E is the external
 electric field strength. For the conventional plasmonic nanoantenna, the differential scattering signal displays a linear
 dependence to the applied electric field with 0.28´10-3 nm/mV (Fig. 2b, blue line). The linear relationship in between the
 differential scattering signal and the local electric field strength is associated to the altering plasma frequency of the metal
 [7]. In the case of PEDOT: PSS, following Eqs.1-2, dielectric permittivity modulations can be simply expressed as
 Δε PEDOT ∝ E . The LSP resonance of the electro-plasmonic nanoantenna is extremely sensitive to the external field through
 the PEDOT:PSS load. In our experiments, we showed that demonstrated more than three orders of magnitude enhanced
 sensitivity of 9.1 × 10−5 cm/V for the electro-plasmonic nanoantenna (Fig.2b, red line) [7].

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Figure 3. Electric field sensitivity and scaling of electro-plasmonic field probe. (a) Electric field sensitivity of a 90 nm diameter electro-
 plasmonic nanoantenna. Differential scattering signal (blue-curve) and SSNR (red-curve) are calculated at different distances from the
 cell. We assumed an incident light intensity of 100 W/cm2, an integration time of 1 ms, NA of 0.45, and an overall detection efficiency
 of 50%. (b) Resonance wavelength shift for varying diameters of electro-plasmonic voltage probes are calculated using Eq. 1. Here, we
 use E=150 V/cm (~ 100 µm from the cell), ! =1.79 pHz, Qsca =5.6 and "#$%& =1.43 pHz [28]. L is calculated analytically [29].

 Next, we sought to establish detection limits of our electro-plasmonic nanoantenna. The optical shot noise provides a
 fundamental bottleneck for optical measurements with low photon counts [e.g., the genetically encoded voltage indicators
 (GEVI) with tiny cross-sections and low quantum yield]. The photon counts need to be boosted to achieve high signal-to-
 shot-noise ratio measurements. Electro-plasmonic nanoantennas have physically much larger dimensions (90 nm in
 diameter), with approximately 10-million times large larger cross-sections compared to those of GEVI [23, 30]. In addition,
 the LSP controlled light scattering of the loaded nanoantenna results in a high incident to scattered light conversion
 efficiencies. We calculate the SSNR with the following relationship using experimentally obtained (DS/So)EP and 3-D
 FDTD simulations [7]:
 EP
 ⎛ λ ⎞ ⎛ ΔS ⎞
 ( )
 SSNR = QE ⎡⎣ηcollectionT ⎤⎦ I inc Qscatπ r 2 tint ⎜ ⎟ ⎜
 ⎝ hc ⎠ ⎝ S0 E ⎟⎠
 E (2)

 where hcollection is the solid angle fraction of the total scattered light collected by the microscope objective, T is the
 transmittance of the objective lens at the scattering wavelength, QE is the quantum efficiency of the photodetector at the
 scattering wavelength, Iinc is the incident light intensity, Qsca is the scattering efficiency (calculated using FDTD
 simulations), r is the radius of the electro-plasmonic nanoantenna, and tint is the integration time. hcollection , the solid angle
 fraction of the total scattered light collected by the microscope objective, is given by [31]

 ⎛ 2⎞
 1⎜ ⎛ NA ⎞
 ηcollection = 1− 1− ⎜ ⎟ (3)
 ⎟
 2⎜ ⎝ ncoup ⎠ ⎟
 ⎝ ⎠

 where NA is the numerical aperture of the objective, and ncoup is the refractive index of the objective lens coupling medium.

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Our analysis shows that label-free optical detection of cell action potentials is possible with a remarkably high SSNR of
 >250 under typical illumination conditions (100 W/cm2). This measurement capability, outperforming millions of
 genetically tagged voltage sensitive dyes [24], could open the door to extracellular voltage imaging from diffraction limited
 volumes without averaging [7]. Moreover, electro-plasmonic nanoantenna detects electric fields in a similar fashion to
 extracellular microelectrodes without physical contact to the origin of the electrophysiological activity of the electrogenic
 cell. Our analysis indicates that electro-plasmonic nanoantenna can remotely measure the activity of excitable cells from
 distances up to 100 µm in a similar manner as extracellular microelectrodes (Fig. 3a, blue curve). Further improvements
 in photon counts and SSNRs could be achieved by packing electro-plasmonic nanoantenna closely. Scaling of the electro-
 plasmonic nanoantenna dimensions to achieve higher filling factors moderately affect the electric-field sensitivities (Fig.
 3b). However, below 50 nm diameter, rapid scaling of nanoantenna scattering cross-section ( Cscat ∝ a6 ) with nanoantenna
 diameter ( ) poses a fundamental limitation as the photon counts drop significantly.

 Figure 4. Spectroelectrochemical characterization of the electro-plasmonic voltage probe. (a). Experimental scheme used for the dark-
 field spectroelectrochemical measurements. (b) Dynamic response of the electro-plasmonic field probe (red) due to the alternating (1
 kHz) external field (blue).

 We conduct spectroelectrochemical measurements using a transmission dark-field microscope and probe high bandwidth
 measurement capabilities of our electro-plasmonic voltage probe (Figure 4a). Figure 4b shows that our electro-plasmonic
 field probe can closely follow alternating external field with 1kHz frequency.
 For electrophysiological testing, cardiac muscle cells (CMs) are seeded on the electro-plasmonic nanoantenna array (Fig.
 5a). Transmission dark-field measurements are carried out with a compact spectrometer at a fixed integration time of 50
 ms (Fig. 4a). We performed our experiments using light intensities (11 mW/mm2) that are ~102-103 times lower than the
 typical light intensities used in electrophysiological experiments with GEVIs [24]. Our results show that synchronized
 spiking of the CMs leads to increased light scattering (Fig. 5b). To confirm the synchronized behavior, we characterize the
 phenotype of the cells through immunostaining Cardiac Troponin I (cardiomyocyte marker, green), and Connexin 43 (gap
 junction marker, red) (Fig. 5c). In figure 5c, cardiomyocyte marker confirms that the all cells seeded on electro-plasmonic
 nanoantenna are CMs (no cardiac fibroblast cell). Also, gap junction marker displays that the CMs are electrically coupled
 and coupling is mediated by gap junction protein (Connexin units) [32].

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Figure 5. Optoelectrochemical characterization of the electro-plasmonic field probe. (a). SEM micrograph of the cardiac muscle cells
 cultured on electro-plasmonic nanoantenna array (b Differential scattering signal DS/So in response to the electrophysiological activity
 of a network of cardiomyocyte cells. (c) Fluorescence image of Troponin-I (green), and Connexin 43 (red) immunostaining of CMs
 seeded on electro-plasmonic nanoantennas.

 4. CONCLUSIONS
 We have developed a new all-optical, label free, high-throughput, and non-invasive voltage probe to measure the
 electrophysiological activity of the electrogenic cell based on electrochromic loading of the plasmonic nanoantenna.
 Differential scattering signal of the electro-plasmonic nanoantenna is very sensitive to the local electric field due to the
 strong light-localization beyond the diffraction limit and low electron densities of the electrochromic loading material. In
 our experiments, we observed three orders of magnitude enhanced sensitivities with respect to previous all-optical voltage
 probes and high-SSNRs without averaging.

 5. ACKNOWLEDGMENTS

 This work is supported by National Science Foundation grants ECCS-1611290, ECCS-1611083, ECCS-1847733
 (CAREER Award) and CBET-1651385 (CAREER Award). The authors acknowledge Dr. Tom Yuzvinsky (UCSC) for
 his assistance with device fabrication, the W.M. Keck Center for Nanoscale Optofluidics for the use of the FEI Quanta 3D,
 and Imran Hossain (UCSC) for help in setting up the optical measurement systems and technical assistance.

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