Hitchhiker’s Guide to Voltammetry: Acute and Chronic Electrodes for in Vivo Fast-Scan Cyclic Voltammetry

Abstract

Fast-scan cyclic voltammetry (FSCV) has been used for over 20 years to study rapid neurotransmission in awake and behaving animals. These experiments were first carried out with carbon-fiber microelectrodes (CFMs) encased in borosilicate glass, which can be inserted into the brain through micromanipulators and guide cannulas. More recently, chronically implantable CFMs constructed with small diameter fused-silica have been introduced. These electrodes can be affixed in the brain with minimal tissue response, which permits longitudinal measurements of neurotransmission in single recording locations during behavior. Both electrode designs have been used to make novel discoveries in the fields of neurobiology, behavioral neuroscience, and psychopharmacology. The purpose of this Review is to address important considerations for the use of FSCV to study neurotransmitters in awake and behaving animals, with a focus on measurements of striatal dopamine. Common issues concerning experimental design, data collection, and calibration are addressed. When necessary, differences between the two methodologies (acute vs chronic recordings) are discussed. The topics raised in this Review are particularly important as the field moves beyond dopamine toward new neurochemicals and brain regions.

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    Hermans A, Keithley RB, Kita JM, Sombers LA, Wightman RM. Dopamine detection with fast-scan cyclic voltammetry used with analog background subtraction. Anal Chem. 2008;80:4040-4048.

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99. 99.

    Collins AL, Greenfield VY, Bye JK, Linker KE, Wang AS, Wassum KM. Dynamic mesolimbic dopamine signalingduring action sequence learning and expectation violation. Sci Rep. 2016;6:20231.

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     Clark JJ, Collins AL, Sanford CA, Phillips PE. Dopamine encoding of Pavlovian incentive stimuli diminishes with extended training. J Neurosci. 2013;33:3526-3532.

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101. 101.

     Ewing AG, Wightman RM, Dayton MA. In vivo voltammetry with electrodes that discriminate between dopamine and ascorbate. Brain Res. 1982;249:361-370.

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     Gonon F, Buda M, Cespuglio R, Jouvet M. Voltammetry in the striatum of chronic freely moving rats: detection of catechols and ascorbic acid. Brain Res. 1981;223:69-80.

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     Garris PA, Collins LB, Jones SR, Wightman RM. Evoked extracellular dopamine in vivo in the medial prefrontal cortex. J Neurochem. 1993;61:637-647.

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104. 104.

     Jones SR, Mickelson GE, Collins LB, Kawagoe KT, Wightman RM. Interference by pH and Ca2+ ions during measurements of catecholamine release in slices of rat amygdala with fast-scan cyclic voltammetry. J Neurosci Methods. 1994;52:1-10.

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105. 105.

     Kawagoe KT, Garris PA, Wightman RM. Ph-Dependent Processes at Nafion(R)-Coated Carbon-Fiber Micro-electrodes. J Electroanal Chem. 1993;359:193-207.

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106. 106.

     Takmakov P, Zachek MK, Keithley RB, Bucher ES, McCarty GS, Wightman RM. Characterization of local pH changes in brain using fast-scan cyclic voltammetry with carbon microelectrodes. Anal Chem. 2010;82:9892-9900.

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107. 107.

     Rice ME, Nicholson C. Measurement ofnanomolar dopamine diffusion using low-noise perfluorinated ionomercoated carbon fiber microelectrodes and high-speed cyclic voltammetry. Anal Chem. 1989;61:1805-1810.

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108. 108.

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109. 109.

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110. 110.

     Troyer KP, Heien ML, Venton BJ, Wightman RM. Neurochemistry and electroanalytical probes. Curr Opin Chem Biol. 2002;6:696-703.

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111. 111.

     Cheer JF, Wassum KM, Heien ML, Phillips PE, Wightman RM. Cannabinoids enhance subsecond dopamine release in the nucleus accumbens of awake rats. J Neurosci. 2004;24:4393-4400.

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112. 112.

     Venton BJ, Michael DJ, Wightman RM. Correlation of local changes in extracellular oxygen and pH that accompany dopaminergic terminal activity in the rat caudate-putamen. J Neurochem. 2003;84:373-381.

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113. 113.

     Robinson DL, Venton BJ, Heien ML, Wightman RM. Detecting subsecond dopamine release with fast-scan cyclic voltammetry in vivo. Clin Chem. 2003;49:1763-1773.

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114. 114.

     Borland LM, Michael AC. Voltammetric study of the control of striatal dopamine release by glutamate. J Neurochem. 2004;91:220-229.

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115. 115.

     Kramer R. Chemometric Techniques for Quantitative Analysis. 1998.

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116. 116.

     Bro R. Multivariate calibration - What is in chemometrics for the analytical chemist? Anal Chim Acta. 2003;500:185-194.

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117. 117.

     Lavine BK, Workman J. Chemometrics. Anal Chem. 2013;85:705-714.

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118. 118.

     Yorgason JT, Espana RA, Jones SR. Demon voltammetry and analysis software: analysis of cocaine-induced alterations in dopamine signaling using multiple kinetic measures. J Neurosci Methods. 2011;202:158-164.

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119. 119.

     Kishida KT, Saez I, Lohrenz T, Witcher MR, Laxton AW, Tatter SB, White JP, Ellis TL, Phillips PE, Montague PR. Subsecond dopamine fluctuations in human striatum encode superposed error signals about actual and counterfactual reward. Proc Natl Acad Sci U S A. 2016;113:200-205.

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120. 120.

     Keithley RB, Heien ML, Wightman RM. Multivariate concentration determination using principal component regression with residual analysis. TrAC, Trends Anal Chem. 2009;28:1127-1136.

     Not in our library10.1016/j.trac.2009.07.002

121. 121.

     Keithley RB, Heien ML, Wightman RM. Erratum to “Multivariate concentration determination using principal component regression with residual analysis”;. TrAC, Trends Anal Chem. 2010;29:110-110.

     Not in our library10.1016/j.trac.2009.07.002

122. 122.

     Keithley RB, Carelli RM, Wightman RM. Rank estimation and the multivariate analysis of in vivo fast-scan cyclic voltammetric data. Anal Chem. 2010;82:5541-5551.

     Not in our library10.1021/ac100413t

123. 123.

     Keithley RB, Wightman RM. Assessing principal component regression prediction of neurochemicals detected with fast-scan cyclic voltammetry. ACS Chem Neurosci. 2011;2:514-525.

     Not in our library10.1021/cn200035u

124. 124.

     Bucher ES, Brooks K, Verber MD, Keithley RB, Owesson-White C, Carroll S, Takmakov P, McKinney CJ, Wightman RM. Flexible software platform for fast-scan cyclic voltammetry data acquisition and analysis. Anal Chem. 2013;85:10344-10353.

     Not in our library10.1021/ac402263x

125. 125.

     Rodeberg NT, Johnson JA, Cameron CM, Saddoris MP, Carelli RM, Wightman RM. Construction of Training Sets for Valid Calibration of in Vivo Cyclic Voltammetric Data by Principal Component Analysis. Anal Chem. 2015;87:11484-11491.

     Not in our library10.1021/acs.analchem.5b03222

126. 126.

     Johnson JA, Rodeberg NT, Wightman RM. Failure of Standard Training Sets in the Analysis of Fast-Scan Cyclic Voltammetry Data. ACS Chem Neurosci. 2016;7:349-359.

     Not in our library10.1021/acschemneuro.5b00302

127. 127.

     Malinowski ER. Determination of Number of Factors and Experimental Error in a Data Matrix. Anal Chem. 1977;49:612-617.

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128. 128.

     Malinowski ER. Adaptation of the Vogt-Mizaikoff F-test to determine the number of principal factors responsible for a data matrix and comparison with other popular methods. J Chemom. 2004;18:387-392.

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129. 129.

     Adams D. The Hitchhiker's Guide to the Galaxy. 1980.

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130. 130.

     Jackson JE, Mudholkar GS. Control Procedures for Residuals Associated with Principal Component Analysis. Technometrics. 1979;21:341-349.

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131. 131.

     Garris PA, Wightman RM. Different kinetics govern dopaminergic transmission in the amygdala, prefrontal cortex, and striatum: an in vivo voltammetric study. J Neurosci. 1994;14:442-450.

     Not in our library10.1523/jneurosci.14-01-00442.1994

132. 132.

     Dengler AK, Wightman RM, McCarty GS. Microfabricated Collector-Generator Electrode Sensor for Measuring Absolute pH and Oxygen Concentrations. Anal Chem. 2015;87:10556-10564.

     Not in our library10.1021/acs.analchem.5b02866

133. 133.

     Cheer JF, Aragona BJ, Heien ML, Seipel AT, Carelli RM, Wightman RM. Coordinated accumbal dopamine release and neural activity drive goal-directed behavior. Neuron. 2007;54:237-244.

     Not in our library10.1016/j.neuron.2007.03.021

134. 134.

     Owesson-White CA, Cheer JF, Beyene M, Carelli RM, Wightman RM. Dynamic changes inaccumbens dopamine correlate with learning during intracranial self-stimulation. Proc Natl Acad Sci U S A. 2008;105:11957-11962.

     Not in our library10.1073/pnas.0803896105

135. 135.

     Park J, Bucher ES, Fontillas K, Owesson-White C, Ariansen JL, Carelli RM, Wightman RM. Opposing catecholamine changes in the bed nucleus of the stria terminalis during intracranial self-stimulation and its extinction. Biol Psychiatry. 2013;74:69-76.

     Not in our library10.1016/j.biopsych.2012.11.008

136. 136.

     Garris PA, Budygin EA, Phillips PE, Venton BJ, Robinson DL, Bergstrom BP, Rebec GV, Wightman RM. A role for presynaptic mechanisms in the actions of nomifensine and haloperidol. Neuroscience. 2003;118:819-829.

     Not in our library10.1016/s0306-4522(03)00005-8

137. 137.

     Wanat MJ, Kuhnen CM, Phillips PE. Delays conferred by escalating costs modulate dopamine release to rewards but not their predictors. J Neurosci. 2010;30:12020-12027.

     Not in our library10.1523/jneurosci.2691-10.2010

138. 138.

     De Noord OE. Multivariate calibration standardization. Chemom Intell Lab Syst. 1994;25:85-97.

     Not in our library

139. 139.

     Feudale RN, Woody NA, Tan H, Myles AJ, Brown SD, Ferre J. Transfer of multivariate calibration models: a review. Chemom Intell Lab Syst. 2002;64:181-192.

     Not in our library

140. 140.

     Schultz W, Dayan P, Montague PR. A neural substrate of prediction and reward. Science. 1997;275:1593-1599.

     Not in our library10.1126/science.275.5306.1593

141. 141.

     Bayer HM, Lau B, Glimcher PW. Statistics of midbrain dopamine neuron spike trains in the awake primate. J Neurophysiol. 2007;98:1428-1439.

     Not in our library10.1152/jn.01140.2006

142. 142.

     Kobayashi S, Schultz W. Influence of reward delays on responses of dopamine neurons. J Neurosci. 2008;28:7837-7846.

     Not in our library10.1523/jneurosci.1600-08.2008

143. 143.

     Fiorillo CD, Newsome WT, Schultz W. The temporal precision of reward prediction in dopamine neurons. Nat Neurosci. 2008;11:966-973.

     Not in our library10.1038/nn.2159

144. 144.

     Nasrallah NA, Clark JJ, Collins AL, Akers CA, Phillips PE, Bernstein IL. Risk preference following adolescent alcohol use is associated with corrupted encoding of costs but not rewards by mesolimbic dopamine. Proc Natl Acad Sci U S A. 2011;108:5466-5471.

     Not in our library10.1073/pnas.1017732108

145. 145.

     Sugam JA, Day JJ, Wightman RM, Carelli RM. Phasic nucleus accumbens dopamine encodes risk-baseddecision-making behavior. Biol Psychiatry. 2012;71:199-205.

     Not in our library10.1016/j.biopsych.2011.09.029

146. 146.

     Lak A, Stauffer WR, Schultz W. Dopamine prediction error responses integrate subjective value from different reward dimensions. Proc Natl Acad Sci U S A. 2014;111:2343-2348.

     Not in our library10.1073/pnas.1321596111

147. 147.

     Gan JO, Walton ME, Phillips PEM. Dissociable cost and benefit encoding of future rewards by mesolimbic dopamine. Nat Neurosci. 2010;13:25-27.

     Not in our library10.1038/nn.2460

148. 148.

     Pasquereau B, Turner RS. Limited encoding of effort by dopamine neurons in a cost-benefit trade-off task. J Neurosci. 2013;33:8288-8300.

     Not in our library10.1523/jneurosci.4619-12.2013

149. 149.

     Fiorillo CD, Tobler PN, Schultz W. Discrete coding of reward probability and uncertainty by dopamine neurons. Science. 2003;299:1898-1902.

     Not in our library10.1126/science.1077349

150. 150.

     Hart AS, Clark JJ, Phillips PE. Dynamic shaping of dopamine signals during probabilistic Pavlovian conditioning. Neurobiol Learn Mem. 2015;117:84-92.

     Not in our library10.1016/j.nlm.2014.07.010

151. 151.

     Waelti P, Dickinson A, Schultz W. Dopamine responses comply with basic assumptions of formal learning theory. Nature. 2001;412:43-48.

     Not in our library10.1038/35083500

152. 152.
     Dopamine Reward Prediction Error Responses Reflect Marginal Utility · 2014

     No notice
153. 153.

     Saddoris MP, Sugam JA, Carelli RM. Prior Cocaine Experience Impairs Normal Phasic Dopamine Signals of Reward Value in Accumbens Shell. Neuropsychopharmacology. 2017;42:766.

     Not in our library10.1038/npp.2016.189

154. 154.

     Soto RJ, Schoenfisch MH. Preclinical Performance Evaluation of Percutaneous Glucose Biosensors: Experimental Considerations and Recommendations. J Diabetes Sci Technol. 2015;9:978-984.

     Not in our library10.1177/1932296815590628

155. 155.

     Dankoski EC, Wightman RM. Monitoring serotonin signaling on a subsecond time scale. Front Integr Neurosci. 2013;7:44.

     Not in our library10.3389/fnint.2013.00044

156. 156.

     Fox ME, Studebaker RI, Swofford NJ, Wightman RM. Stress and Drug Dependence Differentially Modulate Norepinephrine Signaling in Animals with Varied HPA Axis Function. Neuropsychopharmacology. 2015;40:1752-1761.

     Not in our library10.1038/npp.2015.23

157. 157.

     Spanos M, Gras-Najjar J, Letchworth JM, Sanford AL, Toups JV, Sombers LA. Quantitation of hydrogen peroxide fluctuations and their modulation of dopamine dynamics in the rat dorsal striatum using fast-scan cyclic voltammetry. ACS Chem Neurosci. 2013;4:782-789.

     Not in our library10.1021/cn4000499

158. 158.

     Swamy BE, Venton BJ. Subsecond detection of physiological adenosine concentrations using fast-scan cyclic voltammetry. Anal Chem. 2007;79:744-750.

     Not in our library10.1021/ac061820i

Cited by papers we hold 1

• A dopaminergic switch for fear to safety transitions · 2018
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