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Deep Brain Stimulation Macroelectrodes Compared To Deep brain stimulation macroelectrodes compared to multiple microelectrodes in rat hippocampus Sharanya Arcot Desai, Georgia Institute of Technology Claire-Anne Gutekunst, Emory University Steve Potter, Emory University Robert Gross, Emory University Journal Title: Frontiers in Neuroengineering Volume: Volume 7, Number JUN Publisher: Frontiers Media | 2014-06-12, Pages 16-16 Type of Work: Article | Final Publisher PDF Publisher DOI: 10.3389/fneng.2014.00016 Permanent URL: https://pid.emory.edu/ark:/25593/rsb7b Final published version: http://dx.doi.org/10.3389/fneng.2014.00016 Copyright information: © 2014 Arcot Desai, Gutekunst, Potter and Gross. This is an Open Access work distributed under the terms of the Creative Commons Attribution 3.0 Unported License (http://creativecommons.org/licenses/by/3.0/). Accessed September 25, 2021 7:22 PM EDT ORIGINAL RESEARCH ARTICLE published: 12 June 2014 doi: 10.3389/fneng.2014.00016 Deep brain stimulation macroelectrodes compared to multiple microelectrodes in rat hippocampus Sharanya Arcot Desai 1,2 , Claire-Anne Gutekunst 3 , Steve M. Potter 1,2 *† and Robert E. Gross 2,3 *† 1 Laboratory for Neuroengineering, Georgia Institute of Technology, Atlanta, GA, USA 2 The Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology, Atlanta, GA, USA 3 Department of Neurosurgery, Emory University School of Medicine, Atlanta, GA, USA Edited by: Microelectrode arrays (wire diameter <50 μm) were compared to traditional macroelec- Laura Ballerini, University of Trieste, trodes for deep brain stimulation (DBS). Understanding the neuronal activation volume may Italy help solve some of the mysteries associated with DBS, e.g., its mechanisms of action. We Reviewed by: used c-fos immunohistochemistry to investigate neuronal activation in the rat hippocampus Luca Berdondini, Italian Institute of Technology, Italy caused by multi-micro- and macroelectrode stimulation. At ± 1V stimulation at 25 Hz, Vassiliy Tsytsarev, University of microelectrodes (33 μm diameter) had a radius of activation of 100 μm, which is 50% of Maryland School of Medicine, USA that seen with 150 μm diameter macroelectrode stimulation. Macroelectrodes activated *Correspondence: about 5.8 times more neurons than a single microelectrode, but displaced ∼20 times Steve M. Potter, Laboratory for more neural tissue. The sphere of influence of stimulating electrodes can be significantly Neuroengineering, Georgia Institute of Technology, 313 Ferst Drive, increased by reducing their impedance. By ultrasonic electroplating (sonicoplating) the Atlanta, GA 30332, USA microelectrodes with platinum to increase their surface area and reduce their impedance e-mail: [email protected]; by an order of magnitude, the radius of activation increased by 50 μm and more than Robert E. Gross, Department of Neurosurgery, Emory University twice the number of neurons were activated within this increased radius compared to School of Medicine, Suite 6329, unplated microelectrodes. We suggest that a new approach to DBS, one that uses multiple 101 Woodruff Circle, Atlanta, GA high-surface area microelectrodes, may be more therapeutically effective due to increased 30322, USA neuronal activation. e-mail: [email protected] †Steve M. Potter and Robert E. Gross Keywords: deep brain stimulation, neuronal activation, immediate early gene (IEG), multielectrode array (MEA), have contributed equally to this work. macroelectrodes, hippocampus, electroplating INTRODUCTION stimulation not possible with a single macroelectrode. Third, While beneficial for neuropsychiatric disorders spanning a wide tissue damage by MEAs may be less than that caused by macro- range (e.g., Parkinson’s disease, depression, epilepsy), much electrodes. The first goal of this study was to compare the remains to be learned about the mechanisms of action of deep volume of tissue activated by multimicroelectrode arrays and brain stimulation (DBS; Kumar et al., 1998; McIntyre et al., single macroelectrodes. 2004b; Mayberg et al., 2005; Greenberg et al., 2006; Perlmutter Reducing the impedance of microelectrodes provides several and Mink, 2006; Volkmann et al., 2006; Benabid et al., 2009). advantages for neural recording, such as reduced stimulation arti- In particular, a greater understanding the spatial extent of fact and reduced thermal noise leading to improved signal to noise influence of electrical stimulation and the factors that deter- ratio (Ferguson et al., 2009; Desai et al., 2010). For microstimula- mine it is required to optimize the effectiveness and efficiency tion, stimulation amplitude is limited to 1 V due to the possibility of DBS. of water hydrolysis, which therefore limits current density and thus All clinical DBS electrodes are single macroelectrodes, cylindri- stimulation effectiveness (Rozman et al., 2000). Thus, impedance cal in shape with diameters ∼1 mm and surface areas ∼6mm2, reduction allows for achieving higher currents in both voltage and although arrays of multiple smaller electrodes have been proposed. current-controlled applications at the near-maximum of safe volt- However, stimulation through multielectrode arrays (MEA) of ages. A second goal of this study was to compare volume of tissue microelectrodes (i.e., microstimulation; Desai et al., 2010)may activated with untreated microelectrodes to that attained in elec- have advantages when compared to single macroelectrode stim- troplated microelectrodes that are coated to reduce impedance ulation (i.e., macrostimulation) for several reasons, especially (Desai et al., 2010). when stimulating complex structures like the hippocampus, an Several simulation studies by Grill (1999), McIntyre et al. important locus in the etiology of temporal lobe epilepsy (Velasco (2004a), Wei and Grill (2009), Chaturvedi et al. (2010), But- et al., 2001, 2007). First, microelectrodes with diameters of 10s son et al. (2011), and others have estimated the electrical fields of microns can be specifically targeted toward particular cell lay- and activating functions surrounding electrode tracks, but this ers, which may not be possible with a macroelectrode whose needs validation in living neuronal tissue. An excellent study diameter (e.g., 1.27 mm) is bigger than these targets. Second, by Histed et al. (2009) used 2-photon calcium imaging to study one or a few microelectrodes within a MEA may be stimu- patterns of cell activation using microelectrodes in the superfi- lated at a time, which would enable spatiotemporal patterns of cial layers of cortex. Although this technique has great temporal Frontiers in Neuroengineering www.frontiersin.org June 2014 | Volume 7 | Article 16 | 1 Arcot Desai et al. DBS macro vs. microelectrodes and spatial resolution, it cannot be used in deep brain struc- diameter, Plastics One, VA, USA) aimed toward the CA3 cell tures like thalamus or hippocampus because brain tissue strongly layer of the dorsal hippocampus. Rats in groups 2 and 3 were scatters light and imaging becomes impossible beyond a depth implanted with a microelectrode array (Tucker-Davis Technolo- of1mm(Helmchen and Denk, 2005). The results from the gies, FL, USA) with 16 33-μm diameter electrodes arranged in Histed et al. (2009) study will certainly serve as a guiding point tworowsof8(Figure 1). Row 1 was targeted toward the CA1 for understanding electrical stimulation interaction with neu- cell layer and row 2 was targeted toward the CA3 cell layer of ronal populations, but cannot be directly translated to other the dorsal hippocampus. Whereas group 2 had unplated micro- brain regions which have different cytoarchitecture and projection electrodes implanted, the microelectrodes in group 3 had their patterns. impedances reduced by an order of magnitude by sonicoplating c-fos is an immediate early gene which has been used exten- with platinum black (Desai et al., 2010). Sonicoplating (electro- sively as a metabolic marker to study seizure pathways and plating under ultrasonic vibrations) significantly improves the neuroanatomical connections, and to analyze neuronal popula- durability of platinum black on the base metal. Details on this tions activated by a wide range of stimuli including neuroactive procedure and its effect on recording and stimulation perfor- drugs and brain stimulation techniques (Dragunow and Faull, mance of the microelectrode in chronic implants can be found 1989; Saryyeva et al., 2011). Transient induction of c-fos mRNA elsewhere (Desai et al., 2010). Shown in Figure 2 are impedance and protein has been reported in several studies following neu- plots of a macroelectrode and microelectrode array before and ronal excitation (Morgan and Curran, 1991). The mRNA reaches after electroplating. Since microelectrodes in the MEA were con- peak values at 30–45 min post-stimulation and decays with a half- nected in parallel while being stimulated, it was necessary to life of 12 min. c-fos protein synthesis follows mRNA expression make sure that the combined impedance of 15 microelectrodes and it is turned over with a half-life of about2h(Muller et al., (with and without electroplating) did not fall below 200 1984). Given these long activation and decay time scales, this tech- since the maximum current delivering capacity of our setup is nique lacks temporal resolution. However, it provides single-cell ±5 mA and we used ±1V voltage controlled stimulation in our spatial resolution and can be used to visualize and count indi- study. vidual neurons activated by electrical stimulation as shown in Saryyeva et al.
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