Dopamine Dynamics During Continuous Intracranial Self-Stimulation: Effect of Waveform on Fast-Scan Cyclic Voltammetry Data

Overview

Journal ACS Chem Neurosci

Publisher American Chemical Society

Specialty Neurology

Date 2016 Aug 23

PMID 27548680

Citations 11

Authors

Nathan T Rodeberg

Justin A Johnson

Elizabeth S Bucher

R Mark Wightman

Affiliations

Soon will be listed here.

Abstract

The neurotransmitter dopamine is heavily implicated in intracranial self-stimulation (ICSS). Many drugs of abuse that affect ICSS behavior target the dopaminergic system, and optogenetic activation of dopamine neurons is sufficient to support self-stimulation. However, the patterns of phasic dopamine release during ICSS remain unclear. Early ICSS studies using fast-scan cyclic voltammetry (FSCV) rarely observed phasic dopamine release, which led to the surprising conclusion that it is dissociated from ICSS. However, several advances in the sensitivity (i.e., the use of waveforms with extended anodic limits) and analysis (i.e., principal component regression) of FSCV measurements have made it possible to detect smaller, yet physiologically relevant, dopamine release events. Therefore, this study revisits phasic dopamine release during ICSS using these tools. It was found that the anodic limit of the voltammetric waveform has a substantial effect on the patterns of dopamine release observed during continuous ICSS. While data collected with low anodic limits (i.e., +1.0 V) support the disappearance of phasic dopamine release observed in previous investigation, the use of high anodic limits (+1.3 V, +1.4 V) allows for continual detection of dopamine release throughout ICSS. However, the +1.4 V waveform lacks the ability to resolve narrowly spaced events, with the best balance of temporal resolution and sensitivity provided by the +1.3 V waveform. Ultimately, it is revealed that the amplitude of phasic dopamine release decays but does not fully disappear during continuous ICSS.

Citing Articles

Nigrostriatal dopamine signals sequence-specific action-outcome prediction errors.

Hollon N, Williams E, Howard C, Li H, Traut T, Jin X Curr Biol. 2021; 31(23):5350-5363.e5.

PMID: 34637751 PMC: 8665080. DOI: 10.1016/j.cub.2021.09.040.

Acupuncture Modulates Intracranial Self-Stimulation of the Medial Forebrain Bundle in Rats.

Yoon S, Yun J, Lee B, Kim H, Yang C Int J Mol Sci. 2021; 22(14).

PMID: 34299139 PMC: 8304740. DOI: 10.3390/ijms22147519.

Mitigating the Effects of Electrode Biofouling-Induced Impedance for Improved Long-Term Electrochemical Measurements In Vivo.

Seaton B, Hill D, Cowen S, Heien M Anal Chem. 2020; 92(9):6334-6340.

PMID: 32298105 PMC: 8281608. DOI: 10.1021/acs.analchem.9b05194.

Recent advances in fast-scan cyclic voltammetry.

Puthongkham P, Venton B Analyst. 2020; 145(4):1087-1102.

PMID: 31922162 PMC: 7028521. DOI: 10.1039/c9an01925a.

Electrochemistry at the Synapse.

Shin M, Wang Y, Borgus J, Venton B Annu Rev Anal Chem (Palo Alto Calif). 2019; 12(1):297-321.

PMID: 30707593 PMC: 6989097. DOI: 10.1146/annurev-anchem-061318-115434.

References

Rebec G, Christensen J, Guerra C, Bardo M . Regional and temporal differences in real-time dopamine efflux in the nucleus accumbens during free-choice novelty. Brain Res. 1998; 776(1-2):61-7. DOI: 10.1016/s0006-8993(97)01004-4. View

MICHAEL A, Ikeda M, Justice Jr J . Mechanisms contributing to the recovery of striatal releasable dopamine following MFB stimulation. Brain Res. 1987; 421(1-2):325-35. DOI: 10.1016/0006-8993(87)91302-3. View

Garris P, Kilpatrick M, Bunin M, Michael D, Walker Q, Wightman R . Dissociation of dopamine release in the nucleus accumbens from intracranial self-stimulation. Nature. 1999; 398(6722):67-9. DOI: 10.1038/18019. View

Bielajew C, Shizgal P . Evidence implicating descending fibers in self-stimulation of the medial forebrain bundle. J Neurosci. 1986; 6(4):919-29. PMC: 6568435. View

Singh Y, Sawarynski L, Dabiri P, Choi W, Andrews A . Head-to-head comparisons of carbon fiber microelectrode coatings for sensitive and selective neurotransmitter detection by voltammetry. Anal Chem. 2011; 83(17):6658-66. PMC: 3165139. DOI: 10.1021/ac2011729. View

Kishida K, Saez I, Lohrenz T, Witcher M, Laxton A, Tatter S . Subsecond dopamine fluctuations in human striatum encode superposed error signals about actual and counterfactual reward. Proc Natl Acad Sci U S A. 2015; 113(1):200-5. PMC: 4711839. DOI: 10.1073/pnas.1513619112. View

Heien M, Phillips P, Stuber G, Seipel A, Wightman R . Overoxidation of carbon-fiber microelectrodes enhances dopamine adsorption and increases sensitivity. Analyst. 2004; 128(12):1413-9. DOI: 10.1039/b307024g. View

Gallistel C, Shizgal P, Yeomans J . A portrait of the substrate for self-stimulation. Psychol Rev. 1981; 88(3):228-73. View

You Z, Chen Y, Wise R . Dopamine and glutamate release in the nucleus accumbens and ventral tegmental area of rat following lateral hypothalamic self-stimulation. Neuroscience. 2001; 107(4):629-39. DOI: 10.1016/s0306-4522(01)00379-7. View

10.

Rodeberg N, Johnson J, Cameron C, Saddoris M, Carelli R, Wightman R . Construction of Training Sets for Valid Calibration of in Vivo Cyclic Voltammetric Data by Principal Component Analysis. Anal Chem. 2015; 87(22):11484-91. PMC: 5131642. DOI: 10.1021/acs.analchem.5b03222. View

11.

Park J, Takmakov P, Wightman R . In vivo comparison of norepinephrine and dopamine release in rat brain by simultaneous measurements with fast-scan cyclic voltammetry. J Neurochem. 2011; 119(5):932-44. PMC: 3217157. DOI: 10.1111/j.1471-4159.2011.07494.x. View

12.

Carlezon Jr W, Todtenkopf M, McPhie D, Pimentel P, Pliakas A, Stellar J . Repeated exposure to rewarding brain stimulation downregulates GluR1 expression in the ventral tegmental area. Neuropsychopharmacology. 2001; 25(2):234-41. DOI: 10.1016/S0893-133X(01)00232-9. View

13.

Logman M, Budygin E, Gainetdinov R, Wightman R . Quantitation of in vivo measurements with carbon fiber microelectrodes. J Neurosci Methods. 2000; 95(2):95-102. DOI: 10.1016/s0165-0270(99)00155-7. View

14.

Sombers L, Beyene M, Carelli R, Wightman R . Synaptic overflow of dopamine in the nucleus accumbens arises from neuronal activity in the ventral tegmental area. J Neurosci. 2009; 29(6):1735-42. PMC: 2673986. DOI: 10.1523/JNEUROSCI.5562-08.2009. View

15.

Keithley R, Carelli R, Wightman R . Rank estimation and the multivariate analysis of in vivo fast-scan cyclic voltammetric data. Anal Chem. 2010; 82(13):5541-51. PMC: 2895304. DOI: 10.1021/ac100413t. View

16.

Fiorino D, Coury A, Fibiger H, Phillips A . Electrical stimulation of reward sites in the ventral tegmental area increases dopamine transmission in the nucleus accumbens of the rat. Behav Brain Res. 1993; 55(2):131-41. DOI: 10.1016/0166-4328(93)90109-4. View

17.

Reynolds J, Hyland B, Wickens J . A cellular mechanism of reward-related learning. Nature. 2001; 413(6851):67-70. DOI: 10.1038/35092560. View

18.

Wightman R, Heien M, Wassum K, Sombers L, Aragona B, Khan A . Dopamine release is heterogeneous within microenvironments of the rat nucleus accumbens. Eur J Neurosci. 2007; 26(7):2046-54. DOI: 10.1111/j.1460-9568.2007.05772.x. View

19.

Witten I, Steinberg E, Lee S, Davidson T, Zalocusky K, Brodsky M . Recombinase-driver rat lines: tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron. 2011; 72(5):721-33. PMC: 3282061. DOI: 10.1016/j.neuron.2011.10.028. View

20.

Heien M, Johnson M, Wightman R . Resolving neurotransmitters detected by fast-scan cyclic voltammetry. Anal Chem. 2004; 76(19):5697-704. DOI: 10.1021/ac0491509. View