Wireless transmission of fast-scan cyclic voltammetry at a carbon-fiber microelectrode: proof of principle

Fast-scan cyclic voltammetry (FSCV) at a carbon-fiber microelectrode (CFM) provides exquisite temporal and spatial resolution for monitoring brain chemistry. The utility of this approach has recently been demonstrated by measuring sub-second dopamine changes associated with behavior. However, one drawback is the cable link between animal and recording equipment that restricts behavior and precludes monitoring in complex environments. As a first step towards developing new instrumentation to overcome this technical limitation, the goal of the present study was to establish proof of principle for the wireless transmission of FSCV at a CFM. Proof of principle was evaluated in terms of measurement stability, fidelity, and susceptibility to ambient electrical noise. Bluetooth digital telemetry provided bi-directional communication between remote and home-base units and stable, high-fidelity data transfer comparable to conventional, wired systems when tested using a dummy cell (i.e., a resistor and capacitor in series simulating electrical properties of a CFM), and dopamine measurements with flow injection analysis and in the anesthetized rat with electrical stimulation. The wireless system was also less susceptible to interference from ambient electrical noise. Taken together, the present findings establish proof of principle for the wireless transmission of FSCV at a CFM.

[1]  M D Chen,et al.  Radiotelemetric monitoring of hypothalamic gonadotropin-releasing hormone pulse generator activity throughout the menstrual cycle of the rhesus monkey. , 1991, Endocrinology.

[2]  R. Wightman,et al.  Improving data acquisition for fast-scan cyclic voltammetry. , 1999, Analytical chemistry.

[3]  M. Mancia,et al.  Changes in the serotonergic system during the sleep-wake cycle: Simultaneous polygraphic and voltammetric recordings in hypothalamus using a telemetry system , 1994, Neuroscience.

[4]  L. Imeri,et al.  Miniaturized optoelectronic system for telemetry of in vivo voltammetric signals , 1990, Journal of Neuroscience Methods.

[5]  Martyn G Boutelle,et al.  An amperometric glucose-oxidase/poly(o-phenylenediamine) biosensor for monitoring brain extracellular glucose: in vivo characterisation in the striatum of freely-moving rats , 1998, Journal of Neuroscience Methods.

[6]  C. A. Marsden,et al.  In vivo voltammetry—Present electrodes and methods , 1988, Neuroscience.

[7]  R. Wightman,et al.  Electrochemical, pharmacological and electrophysiological evidence of rapid dopamine release and removal in the rat caudate nucleus following electrical stimulation of the median forebrain bundle. , 1985, European journal of pharmacology.

[8]  P. Garris,et al.  ‘Passive stabilization’ of striatal extracellular dopamine across the lesion spectrum encompassing the presymptomatic phase of Parkinson's disease: a voltammetric study in the 6‐OHDA‐lesioned rat , 2003, Journal of neurochemistry.

[9]  P. Garris,et al.  Real‐Time Measurement of Electrically Evoked Extracellular Dopamine in the Striatum of Freely Moving Rats , 1997, Journal of neurochemistry.

[10]  V. Annovazzi-Lodi,et al.  An optoelectronic link for bidirectional transmission of biological signals , 1988, IEEE Transactions on Biomedical Engineering.

[11]  R. Mark Wightman,et al.  Peer Reviewed: Color Images for Fast-Scan CV Measurements in Biological Systems , 1998 .

[12]  Sam A Deadwyler,et al.  Examination of factors mediating the transition to behaviorally correlated nucleus accumbens cell firing during cocaine self-administration sessions in rats , 1999, Behavioural Brain Research.

[13]  G. Rebec,et al.  Behavior-related modulation of substantia nigra pars reticulata neurons in rats performing a conditioned reinforcement task , 2002, Neuroscience.

[14]  Christoph Pinkwart,et al.  Miniature three-function transmitting system for single neuron recording, wireless brain stimulation and marking , 1987, Journal of Neuroscience Methods.

[15]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[16]  P. Janak,et al.  Neuronal and behavioral correlations in the medial prefrontal cortex and nucleus accumbens during cocaine self-administration by rats , 2000, Neuroscience.

[17]  George V Rebec,et al.  Modeling fast dopamine neurotransmission in the nucleus accumbens during behavior , 2002, Behavioural Brain Research.

[18]  R. Wightman,et al.  Correlation of local changes in extracellular oxygen and pH that accompany dopaminergic terminal activity in the rat caudate–putamen , 2003, Journal of neurochemistry.

[19]  H. Eichenbaum,et al.  Compact miniature microelectrode-telemetry system , 1977, Physiology & Behavior.

[20]  Ralph N. Adams,et al.  In vivo electrochemical measurements in the CNS , 1990, Progress in Neurobiology.

[21]  R. Wightman,et al.  Subsecond dopamine release promotes cocaine seeking , 2003, Nature.

[22]  Babu Subramanyam,et al.  MONITORING MOLECULES IN NEUROSCIENCE , 1991 .

[23]  Andreas Nieder,et al.  Miniature stereo radio transmitter for simultaneous recording of multiple single-neuron signals from behaving owls , 2000, Journal of Neuroscience Methods.

[24]  M. Mancia,et al.  Hypothalamic serotonergic activity correlates better with brain temperature than with sleep–wake cycle and muscle tone in rats , 1999, Neuroscience.

[25]  P. Garris,et al.  Regional Differences in Dopamine Release, Uptake, and Diffusion Measured by Fast-Scan Cyclic Voltammetry , 1995 .

[26]  K. Chergui,et al.  Uptake of Dopamine Released by Impulse Flow in the Rat Mesolimbic and Striatal Systems In Vivo , 1995, Journal of neurochemistry.

[27]  J. A. Jankowski,et al.  Quantitative determination of catecholamines in individual bovine adrenomedullary cells by reversed-phase microcolumn liquid chromatography with electrochemical detection. , 1992, Analytical chemistry.

[28]  R. Wightman,et al.  Fast-scan voltammetry of biogenic amines. , 1988, Analytical chemistry.

[29]  N. Kulagina,et al.  Monitoring glutamate and ascorbate in the extracellular space of brain tissue with electrochemical microsensors. , 1999, Analytical chemistry.

[30]  John R. C Christensen,et al.  Regional and temporal differences in real-time dopamine efflux in the nucleus accumbens during free-choice novelty , 1997, Brain Research.

[31]  R. Wightman,et al.  Differential quantal release of histamine and 5-hydroxytryptamine from mast cells of vesicular monoamine transporter 2 knockout mice. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Alan A. Boulton,et al.  Voltammetric Methods in Brain Systems , 1995 .

[33]  R. Mark Wightman,et al.  Interference by pH and Ca2+ ions during measurements of catecholamine release in slices of rat amygdala with fast-scan cyclic voltammetry , 1994, Journal of Neuroscience Methods.

[34]  Georg M. Klump,et al.  Time course of simultaneous masking in the starling’s auditory forebrain , 1999, Experimental Brain Research.

[35]  P. Garris,et al.  A role for presynaptic mechanisms in the actions of nomifensine and haloperidol , 2003, Neuroscience.

[36]  P. Garris,et al.  Sub-second changes in accumbal dopamine during sexual behavior in male rats , 2001, Neuroreport.

[37]  Carl J. Weisman Essential guide to RF and wireless , 1999 .

[38]  Christine Jorm,et al.  Fast Cyclic Voltammetry in Brain Slices , 1995 .

[39]  R. Wightman,et al.  Fast-scan cyclic voltammetry of 5-hydroxytryptamine. , 1995, Analytical chemistry.

[40]  R. Wightman,et al.  Strategies for low detection limit measurements with cyclic voltammetry. , 1991, Analytical chemistry.

[41]  R. Wightman,et al.  Microelectrodes for the measurement of catecholamines in biological systems. , 1996, Analytical chemistry.

[42]  Eric W. Kristensen,et al.  Dispersion in flow injection analysis measured with microvoltammetric electrodes , 1986 .

[43]  J. Hollerman,et al.  Dopamine neurons report an error in the temporal prediction of reward during learning , 1998, Nature Neuroscience.

[44]  G. Gerhardt,et al.  Self-referencing ceramic-based multisite microelectrodes for the detection and elimination of interferences from the measurement of L-glutamate and other analytes. , 2001, Analytical chemistry.

[45]  P. Garris,et al.  Frequency of Dopamine Concentration Transients Increases in Dorsal and Ventral Striatum of Male Rats during Introduction of Conspecifics , 2002, The Journal of Neuroscience.

[46]  Jerald D. Kralik,et al.  Chronic, multisite, multielectrode recordings in macaque monkeys , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Jonathan A. Stamford,et al.  Fast cyclic voltammetry: improved sensitivity to dopamine with extended oxidation scan limits , 1990, Journal of Neuroscience Methods.

[48]  Jonathan A. Stamford,et al.  In vivo voltammetric characterization of low affinity striatal dopamine uptake: Drug inhibition profile and relation to dopaminergic innervation density , 1986, Brain Research.

[49]  Charles Nicholson,et al.  Diffusion and Ion Shifts in the Brain Extracellular Microenvironment and Their Relevance for Voltammetric Measurements , 1995 .

[50]  A. Michael,et al.  Direct Comparison of the Response of Voltammetry and Microdialysis to Electrically Evoked Release of Striatal Dopamine , 1998, Journal of neurochemistry.

[51]  R. Wightman,et al.  Transient changes in mesolimbic dopamine and their association with ‘reward’ , 2002, Journal of neurochemistry.