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J. Shim (2015)
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Selective inhibition of small-diameter axons using infrared lightScientific Reports, 7
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Control of resting membrane potential by delayed rectifier potassium currents in ferret airway smooth muscle cells.The Journal of Physiology, 469
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Infrared inhibition of embryonic heartsJournal of Biomedical Optics, 21
M. Chernov, Austin Duke, J. Cayce, S. Crowder, H. Sung, E. Jansen (2012)
Material considerations for optical interfacing to the nervous systemMRS Bulletin, 37
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Voltage-gated potassium channels are critical for infrared inhibition of action potentials: an experimental study Mohit Ganguly Jeremy B. Ford Junqi Zhuo Matthew T. McPheeters Michael W. Jenkins Hillel J. Chiel E. Duco Jansen Mohit Ganguly, Jeremy B. Ford, Junqi Zhuo, Matthew T. McPheeters, Michael W. Jenkins, Hillel J. Chiel, E. Duco Jansen, “Voltage-gated potassium channels are critical for infrared inhibition of action potentials: an experimental study,” Neurophoton. 6(4), 040501 (2019), doi: 10.1117/1.NPh.6.4.040501. NPH Letters There is a need for an alternate modality of neuromodulation Voltage-gated potassium that can mitigate, if not completely eliminate, these disadvan- tages. channels are critical The use of infrared (IR) irradiation on nerves could be one such method. It has been shown that IR light can be used for 5–9 10–14 for infrared inhibition excitation and inhibition of nerves. The technique of IR inhibition of nerves is spatially precise and can be targeted of action potentials: 12 to selectively inhibit axons of smaller diameters. The ability to target axons of small diameters helps motivate IR inhibition an experimental study as a modality that can target finer sensory fibers carrying vital feedback information (e.g., pain, pressure, and temperature sensitivity). Understanding the mechanism of action of IR on a,b a,b c Mohit Ganguly, Jeremy B. Ford, Junqi Zhuo, nerves is critical to exploit the potential of IR inhibition as a c c,d Matthew T. McPheeters, Michael W. Jenkins, clinical modality and optimize its parameter space. It has been c,e,f a,b,g, Hillel J. Chiel, and E. Duco Jansen * shown that heating caused by IR absorption of nerves is respon- Vanderbilt University, Department of Biomedical Engineering, 15–18 sible for inhibition. From simulations using Hodgkin– Nashville, Tennessee, United States 17,18 Vanderbilt University, Biophotonics Center, Nashville, Tennessee, Huxley-based computational models, we hypothesize that United States the mechanism underlying IR inhibition of action potentials is Case Western Reserve University, Department of Biomedical a thermally driven accelerated activation of voltage-gated potas- Engineering, Cleveland, Ohio, United States sium ion channels. This paper tests this hypothesis by studying Case Western Reserve University, Department of Pediatrics, IR nerve inhibition in unmyelinated Aplysia nerves in the pres- Cleveland, Ohio, United States Case Western Reserve University, Department of Biology, ence of voltage-gated ion channel blockers. Cleveland, Ohio, United States Case Western Reserve University, Department of Neurosciences, 2 Methods Cleveland, Ohio, United States Vanderbilt University, Department of Neurological Surgery, Nashville, Tennessee, United States 2.1 Animal Preparation After anesthetizing Aplysia californica (250 to 350 g, Marinus Abstract. Thermal block of unmyelinated axons may Scientific, Long Beach, California) with magnesium chloride serve as a modality for control, suggesting a means for (333 mM, 50% body weight), the right pleural abdominal (PA) providing therapies for pain. Computational modeling nerves were dissected out and suctioned into extracellular predicted that potassium channels are necessary for medi- recording electrodes to record their electrophysiological re- ating thermal block of propagating compound action sponse. The nerves were maintained in room temperature (T ∼ potentials (CAPs) with infrared (IR) light. Our study tests 20°C) Aplysia saline (460 mM NaCl, 10 mM KCl, 22 mM that hypothesis. Results suggest that potassium channel MgCl ,33mM MgSO ,10mM CaCl , 10 mM glucose, 2 4 2 blockers disrupt the ability of IR to block propagating 10 mM HEPES, pH 7.6), which was modified depending on the CAPs in Aplysia californica nerves, whereas sodium chan- type of experiment (see below). Measurements using a cali- nel blockers appear to have no significant effect. These brated microscope done in the laboratory show that the diameter observations validate the modeling results and suggest of the Aplysia PA nerve is 253.09 144.70 μm in diameter potential applications of thermal block to many other unmy- (N ¼ 12, for animals ranging from 250 to 300 g in weight). elinated axons. © The Authors. Published by SPIE under a Creative Commons Attribution 4.0 Unported License. Distribution or reproduction of this work in whole or in part requires full attribution of the original publication, includ- 2.2 Experimental Setup ing its DOI. [DOI: 10.1117/1.NPh.6.4.040501] Nerve-recording electrodes were made by hand-pulling poly- Keywords: infrared inhibition; potassium channels; sodium channels; ethylene tubing (1.27-mm outer diameter, 0.86-mm inner diam- tetraethylammonium chloride; tetrodotoxin. eter) over a flame and cutting them to the desired diameter. Paper 19048LRR received May 21, 2019; accepted for publication Recording electrodes were suction-filled with Aplysia saline Sep. 20, 2019; published online Oct. 15, 2019. prior to suctioning the nerve. Nerve signals were amplified (×10;000) and bandpass filtered (300 to 500 Hz) using an AC-coupled differential amplifier (A-M Systems, Sequim, Washington), digitized using an Axon Digidata 1440A digitizer 1 Introduction (Molecular Devices, San Jose, California), and recorded using Clampex computer software (Molecular Devices, San Jose, Precise control of neural activity (neuromodulation) is a chal- California). Monophasic stimulation current was supplied by lenge that has major scientific and clinical applications for a WPI A365 stimulus isolator (World Precision Instruments, treating and managing symptoms and conditions that are neuro- 1 Sarasota, Florida) for all experiments (stimulation parameters: pathic in origin. Electrical methods of neuromodulation have 200 μA current, τ ¼ 2ms, 1 Hz). The IR block was produced been used for some time but suffer from disadvantages such by a tunable diode laser (Capella Neurostimulator; Lockheed- as lack of selectivity, surgical complications, lead migration, 2,3 Martin-Aculight, Bothell, Washington) with a wavelength of lead breakage, MRI incompatibility, and tolerance buildup. λ ¼ 1875 nm coupled to a 400-μm-diameter multimode optical fiber (Ocean Optics, Dunedin, Florida). The optical fiber was secured in place using micromanipulators. The laser was trig- *Address all correspondence to E. Duco Jansen, E-mail: duco.jansen@ vanderbilt.edu gered at 200 Hz with 200-μs pulses for all experiments. Neurophotonics 040501-1 Oct–Dec 2019 Vol. 6(4) NPH Letters Radiant exposures per pulse at the fiber output were calcu- channels [tetraethylammonium (TEA) chloride] and a blocker lated after measuring the power output using a power meter of voltage-gated sodium ion channels [tetrodotoxin (TTX)]. (Molectron EPM 2000, Coherent, Santa Clara, California). The formulation for TEA saline was 410 mM NaCl, 50 mM The optical fiber was maintained in contact with the nerve sur- TEA, 10 mM KCl, 22 mM MgCl ,33mM MgSO ,10mM 2 4 19,20 face for all irradiation experiments [Fig. 1(a)]. The energy range CaCl , 10 mM glucose, 10 mM HEPES, pH 7.6. Prior 19,20 used in the study was 215.29 19.55 mJ∕cm ∕pulse. studies have shown that TEA blocks both voltage-dependent þ2 A specially designed chamber was fabricated for our experi- and Ca -mediated potassium channels and disrupt potassium ments. The chamber [Fig. 1(b)] consisted of three sections and currents in Aplysia neurons. A solution of 60 μM of TTX was three-dimensional (3-D) printed on a Form 2 printer using saline solution (TTX, Enzo Life Sciences Farmingdale, New black Formlabs Standard Resin (Formlabs Inc., Somerville, York) was prepared by adding 600 μl of 1 mM TTX normal Massachusetts, 50-μm layer height). The sections within the Aplysia saline solution to make a final volume of 10 ml. The chamber were separated using 3-D printed partitions (made concentration of TTX in saline was chosen to be consistent 21–23 of Hewlett-Packard 3-D high reusability polycyclic aromatic with previously published experimental studies in Aplysia. 21–23 12 to provide finer detail). Resin was used for printing since In these studies, it has been observed that use of TTX blocks it provided a good balance between quality and cost. For the inward currents and decreases spiking activity in Aplysia experiments described in this paper, the width of the middle pacemaking and buccal neurons. The effect of all ion channel section (Δx, Fig. 1) was maintained between 2.5 and 3 mm. blockers was reversible, which was confirmed by performing This width is small enough to allow passive currents to propa- recordings after washing out the ion channel blocker solutions. gate past the middle chamber and reinitiate action potentials, The effect of TEA was reversed after 2 to 4 washouts over even in the presence of voltage-gated sodium ion channel block- ∼30 min. The effect of TTX was reversed after 2 to 3 washouts ers. The width was also large enough to allow reliable placement over ∼15 min. The pH of all the saline solutions was adjusted of the optical fiber in contact with the nerve. Leaking was mini- to 7.6, which is the same as that of normal Aplysia saline. All mized by brushing the edges of the partitions with biocompat- solutions were brought to room temperature (T ∼ 20°C) prior to ible Vaseline (Unilever, London/Rotterdam) petroleum jelly to infusion into the chamber. provide a good seal. 2.4 Experimental Protocol 2.3 Channel Blockers and Inhibitors The nerve recording protocol consisted of multiple recordings of To test hypotheses derived from computational modeling 20-s intervals. The nerve was electrically stimulated at a fre- studies, we used a blocker of voltage-gated potassium ion quency of 1 Hz. Each recording consisted of three phases: (1) the time when the laser was off (t ¼ 0 to 5 s), (2) the time when the laser was on (t ¼ 5 to 15 s), and (3) the time when the laser was again off [t ¼ 15 to 20 s; Fig. 2(a)]. Phase 3 of the recording allowed the nerve to recover from the thermal block induced by the IR laser irradiation during the second phase of the record- ing. In each study, the power of the laser was adjusted to obtain a complete block of the compound action potential (CAP) within Fig. 1 Experimental setup. (a) Schematic of experimental setup, which consists of an Aplysia PA connective nerve in a 3-D chamber Fig. 2 Typical IR block. (a) Recording showing IR laser block that consists of three sections (1, 2, and 3). The sections at the obtained when the nerve is in normal Aplysia saline. The laser is ends (shown in blue) contain normal saline. The section in the middle switched on from t ¼ 5 to 15 s and switched off for the last 5 s in each (2, colored red) contains saline solution with or without ion channel recording. (b)–(d) Signals from each phase of the recording are shown blockers. The nerve is irradiated with IR laser radiation delivered in high temporal resolution [(b) preirradiation, (c) during irradiation, via a fiber optic in the middle section. Suction electrodes at the ends and (d) postirradiation]. In each of the high-resolution signals shown, of the nerve allow for stimulation and recording of CAPs (Δx ¼ 2.5 to the electrical recording artifacts are removed. (Laser parameters 3 mm). (b) A schematic showing the layout of the nerve chamber with λ ¼ 1875 nm, optical fiber size ¼ 400 μm, f ¼ 200 Hz, τ ¼ 200 μs, dimensions. and H ¼ 183 mJ∕cm .) Neurophotonics 040501-2 Oct–Dec 2019 Vol. 6(4) NPH Letters the first 5 s after the laser turned on. Once the value of radiant exposure was determined, it was kept constant for the entire duration of a trial. Each trial consisted of three experimental conditions. The trials were conducted in a series of recordings in A-B-A-C-A format. Recording A refers to the observation of nerve activity in the control saline solution (with IR irradiation), before any ion channel blocker is introduced. Recording B refers to the observation of nerve activity in the presence of TEA (with IR irradiation), and recording C refers to the observation of nerve activity in the presence of TTX (with IR irradiation). Experiments were repeated in six different animals (N ¼ 6). 2.4.1 Data acquisition and analysis CAPs were acquired at 50 kHz. Clampex (Molecular Devices, San Jose, California) was used to record acquired data in the computer. After acquisition, data analysis was performed using Fig. 3 Blocking potassium ion channels eliminates IR thermal inhib- a combination of AxoGraph X (Axograph Scientific, Berkeley, ition. High temporal resolution views of representative signals from a California), Matlab (Mathworks, Natick, Massachusetts), nerve undergoing block in the presence of ion channel blockers. Microsoft Excel (Microsoft, Redmond, Washington), and Signals prior to, during, and after laser irradiation in (a)–(c) control Mathematica (Wolfram Inc., Champaign, Illinois). Each record- saline, (e)–(g) TEA, and (i)–(l) TTX are shown. IR-induced thermal ing was divided into three phases [laser off 0 to 5 s, laser on 5 inhibition is observed in (b) control (normal) saline and (j) TTX when the IR laser is switched on. (f) Thermal inhibition is reduced in the to 15 s, and laser off 15 to 20 s, Fig. 2(a)]. The rectified area presence of a potassium channel blocker (TEA chloride). Normal- under the curve (rAUC) was evaluated for signals in each phase ized rAUCs summarizing results from N ¼ 6 observations in (d) con- of the recording. The averages of the areas under “laser off” trol saline, (h) the presence of TEA, and (l) the presence of TTX. Lack phase (phases 1 and 3) were plotted; since they were not signifi- of change in rAUC in TEA is highly significant (see text). cantly different (based on a paired t-test), the ratio of the rAUC in phase 2 relative to phase 1 was computed. For the “laser on” phase (phase 2), rAUC for the signals observed between t ¼ 11 4 Discussion to 15 s of the recordings was measured. Prior studies had indi- The results presented in this paper support the hypothesis cated that the effect of IR takes several seconds to occur, that the primary mechanism by which thermal block occurs is so focusing on the last 5 s of phase 2 ensured that the system due to voltage-dependent potassium ion channels. As shown in had reached a stable state. The areas were normalized to the 17,18 previous modeling studies, in response to heating, voltage- average area calculated for when the laser was off during the dependent potassium channels in unmyelinated axons respond first phase of the recording. Tests for normality were performed more rapidly than they do in unheated axons, generating a using the Shapiro–Wilk test. The data also passed tests for het- hyperpolarizing current in response to depolarizing currents. eroscedasticity so that analysis of variance (ANOVA) could be Results also suggest that sodium channels do not appear to play applied. Posthoc Tukey honest significant difference (HSD) a significant role in establishing a thermal block. Increase in tests were used to determine which changes were statistically activity of potassium channels in mammalian models caused significant at the p ¼ 0.05 level. by accelerated kinetics and increased conductance at elevated 24–26 temperatures have been reported in the literature. Potassium channel blockers have been reported to affect conduction block 3 Results 27–29 at elevated temperatures, but the underlying mechanism has Control experiments using normal saline solutions (without any remained elusive. While all studies mentioned above examined channel blockers) show a block when IR is used on the nerve mammalian systems, to the best of our knowledge, the study [Figs. 2(a)–2(d); Figs. 3(a)–3(d)]. In the presence of TEA, the presented here is the first to highlight the key role of potassium effect of IR in creating a propagation block is greatly reduced channels during thermal block induced by IR laser radiation [Figs. 3(e)–3(h)]. Although TEA prevented laser-induced inhib- in an unmyelinated axon system. These results may lead to ition of the largest CAP units, it still appeared to inhibit smaller, targeted therapies for unmyelinated axons, which carry sensory slower units, which have a lower inhibition threshold, as pre- information such as pain and temperature in a wide range of dicted by modeling results. In the presence of TTX, IR block species, including humans. is again observed [Figs. 3(i)–3(l)]. Overall ANOVA for N ¼ 6 independent experiments shows Disclosures that the overall changes due to the presence of the blockers is −13 No conflicts of interest, financial or otherwise, are declared highly significant (p < 5 × 10 ). Posthoc Tukey HSD tests by the authors. showed that normalized changes in areas of CAPs in saline and TTX (when IR was on, phase 2) relative to control (IR laser off, Acknowledgments phase 1) were not statistically significant, whereas normalized changes in the CAPs in TEA (laser on, phase 2) relative to con- This research was supported by the U.S. Air Force Office of trol (laser off, phase 1) showed no reductions during IR irradi- Sponsored Research (AFOSR) Grant No. FA 9550-17-1-0374 ation and are highly significantly different from the saline and and the U.S. National Institutes of Health (NIH) Grant Nos. −6 TTX results (p < 2 × 10 ). SPARC OT2 OD025307 and R01 HL126747. 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Neurophotonics – SPIE
Published: Oct 1, 2019
Keywords: infrared inhibition; potassium channels; sodium channels; tetraethylammonium chloride; tetrodotoxin
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