Optogenetic versus electrical stimulation of dopamine terminals in the nucleus accumbens reveals local modulation of presynaptic release

Journal of Neurochemistry

Volumn 134, Issue 5, 2015, Pages 833-844

  Melchior, James R ^a   Ferris, Mark J ^a   Stuber, Garret D ^b   Riddle, David R ^c   Jones, Sara R ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c WESTERN MICHIGAN UNIVERSITY HOMER STRYKER MD SCHOOL OF MEDICINE   (United States)

Author keywords

acetylcholine; dopamine; GABA; nucleus accumbens; optogenetics; voltammetry

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; DOPAMINE; NICOTINIC RECEPTOR; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID RECEPTOR; ACETYLCHOLINE; BENZYL[3 [[1 (3,4 DICHLOROPHENYL)ETHYL]AMINO] 2 HYDROXYPROPYL]PHOSPHINIC ACID; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CHANNELRHODOPSIN 2, MOUSE; NERVE PROTEIN; PHOSPHINIC ACID DERIVATIVE; PROPANOLAMINE DERIVATIVE; RHODOPSIN; TYROSINE 3 MONOOXYGENASE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; CYCLIC POTENTIOMETRY; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; ELECTRODE; ELECTROSTIMULATION; MALE; MOUSE; NERVE ENDING; NERVE STIMULATION; NEUROMODULATION; NONHUMAN; NUCLEUS ACCUMBENS; OPTOGENETICS; PHOTOSTIMULATION; PRESYNAPTIC NERVE; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION; ANIMAL; ARTIFACT; BIOSYNTHESIS; C57BL MOUSE; CHOLINERGIC NERVE CELL; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECTS; GENE TARGETING; GENETICS; INTERNEURON; METABOLISM; MICROELECTRODE; PHYSIOLOGY; PROMOTER REGION; SECRETION (PROCESS); SYNAPSE; SYNAPTOSOME; VENTRAL TEGMENTUM;

ACETYLCHOLINE; ANIMALS; ARTIFACTS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CHOLINERGIC NEURONS; DOPAMINE; DOPAMINERGIC NEURONS; ELECTRIC STIMULATION; GABA-B RECEPTOR ANTAGONISTS; GABAERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; GENE KNOCK-IN TECHNIQUES; INTERNEURONS; MALE; MICE; MICE, INBRED C57BL; MICROELECTRODES; NERVE TISSUE PROTEINS; NUCLEUS ACCUMBENS; OPTOGENETICS; PHOSPHINIC ACIDS; PRESYNAPTIC TERMINALS; PROMOTER REGIONS, GENETIC; PROPANOLAMINES; RHODOPSIN; SYNAPSES; TYROSINE 3-MONOOXYGENASE; VENTRAL TEGMENTAL AREA;

EID: 84938957848     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13177     Document Type: Article

References (50)

1. Adamantidis A. R., Tsai H.-C., Boutrel B., Zhang F., Stuber G. D., Budygin E. A., Touriño C., Bonci A., Deisseroth K., and, de Lecea L., (2011) Optogenetic interrogation of dopaminergic modulation of the multiple phases of reward-seeking behavior. J. Neurosci. 31, 10829-10835.
2. Adrover M. F., Shin J. H., and, Alvarez V. A., (2014) Glutamate and dopamine transmission from midbrain dopamine neurons share similar release properties but are differentially affected by cocaine. J. Neurosci. 34, 3183-3192.
3. Bass C. E., Grinevich V. P., Kulikova A. D., Bonin K. D., and, Budygin E. A., (2013) Terminal effects of optogenetic stimulation on dopamine dynamics in rat striatum. J. Neurosci. Methods 214, 149-155.
4. Berthold P., Tsunoda S. P., Ernst O. P., Mages W., Gradmann D., and, Hegemann P., (2008) Channelrhodopsin-1 initiates phototaxis and photophobic responses in chlamydomonas by immediate light-induced depolarization. Plant Cell 20, 1665-1677.
5. Brimblecombe K. R., Gracie C. J., Platt N. J., and, Cragg S. J., (2014) Gating of dopamine transmission by calcium and axonal N-, Q-, T- and L-type voltage-gated calcium channels differs between striatal domains. J. Physiol. 593, 929-946.
6. Cachope R., Mateo Y., Mathur B. N., Irving J., Wang H.-L., Morales M., Lovinger D. M., and, Cheer J. F., (2012) Selective activation of cholinergic interneurons enhances accumbal phasic dopamine release: setting the tone for reward processing. Cell Rep. 2, 33-41.
7. Calipari E. S., Ferris M. J., Melchior J. R., Bermejo K., Salahpour A., Roberts D. C. S., and, Jones S. R., (2014) Methylphenidate and cocaine self-administration produce distinct dopamine terminal alterations. Addict. Biol. 19, 145-155.
8. Charara A., Heilman T. C., Levey A. I., and, Smith Y., (2000) Pre- and postsynaptic localization of GABA(B) receptors in the basal ganglia in monkeys. Neuroscience 95, 127-140.
9. Chaudhury D., Walsh J. J., Friedman A. K., et al,. (2013) Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature 493, 532-536.
10. Citri A., and, Malenka R. C., (2008) Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33, 18-41.
11. Exley R., Clements M. A., Hartung H., McIntosh J. M., and, Cragg S. J., (2008) Alpha6-containing nicotinic acetylcholine receptors dominate the nicotine control of dopamine neurotransmission in nucleus accumbens. Neuropsychopharmacology 33, 2158-2166.
12. Ferris M. J., Calipari E. S., Mateo Y., Melchior J. R., Roberts D. C., and, Jones S. R., (2012) Cocaine self-administration produces pharmacodynamic tolerance: differential effects on the potency of dopamine transporter blockers, releasers, and methylphenidate. Neuropsychopharmacology 37, 1708-1716.
13. Ferris M. J., España R. A., Locke J. L., Konstantopoulos J. K., Rose J. H., Chen R., and, Jones S. R., (2014) Dopamine transporters govern diurnal variation in extracellular dopamine tone. Proc. Natl Acad. Sci. USA 111, E2751-E2759.
14. Grady S. R., Salminen O., Laverty D. C., Whiteaker P., McIntosh J. M., Collins A. C., and, Marks M. J., (2007) The subtypes of nicotinic acetylcholine receptors on dopaminergic terminals of mouse striatum. Biochem. Pharmacol. 74, 1235-1246.
15. Ikemoto S., (2007) Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res. Rev. 56, 27-78.
16. Jones S. R., Gainetdinov R. R., Wightman R. M., and, Caron M. G., (1998) Mechanisms of amphetamine action revealed in mice lacking the dopamine transporter. J. Neurosci. 18, 1979-1986.
17. Margolis E. B., Lock H., Chefer V. I., Shippenberg T. S., Hjelmstad G. O., and, Fields H. L., (2006) Kappa opioids selectively control dopaminergic neurons projecting to the prefrontal cortex. Proc. Natl Acad. Sci. USA 103, 2938-2942.
18. Mateo Y., Lack C. M., Morgan D., Roberts D. C. S., and, Jones S. R., (2005) Reduced dopamine terminal function and insensitivity to cocaine following cocaine binge self-administration and deprivation. Neuropsychopharmacology 30, 1455-1463.
19. Morikawa H., and, Morrisett R. A., (2010) Ethanol action on dopaminergic neurons in the ventral tegmental area: interaction with intrinsic ion channels and neurotransmitter inputs. Int. Rev. Neurobiol. 91, 235-288.
20. Nagel G., Szellas T., Huhn W., Kateriya S., Adeishvili N., Berthold P., Ollig D., Hegemann P., and, Bamberg E., (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl Acad. Sci. USA 100, 13940-13945.
21. Phillips P. E. M., Hancock P. J., and, Stamford J. A., (2002) Time window of autoreceptor-mediated inhibition of limbic and striatal dopamine release. Synapse 44, 15-22.
22. Pitman K. A., Puil E., and, Borgland S. L., (2014) GABAB modulation of dopamine release in the nucleus accumbens core. Eur. J. Neurosci. 40, 3472-3480.
23. Rice M. E., and, Cragg S. J., (2004) Nicotine amplifies reward-related dopamine signals in striatum. Nat. Neurosci. 7, 583-584.
24. Rose J. H., Calipari E. S., Mathews T. A., and, Jones S. R., (2013) Greater ethanol-induced locomotor activation in DBA/2J versus C57BL/6J mice is not predicted by presynaptic striatal dopamine dynamics. PLoS ONE 8, e83852.
25. Schlösser B., Kudernatsch M. B., Sutor B., and, ten Bruggencate G., (1995) Delta, mu and kappa opioid receptor agonists inhibit dopamine overflow in rat neostriatal slices. Neurosci. Lett. 191, 126-130.
26. Schmitz Y., Schmauss C., and, Sulzer D., (2002) Altered dopamine release and uptake kinetics in mice lacking D2 receptors. J. Neurosci. 22, 8002-8009.
27. Schneider F., Gradmann D., and, Hegemann P., (2013) Ion selectivity and competition in channelrhodopsins. Biophys. J. 105, 91-100.
28. Siciliano C. A., Calipari E. S., Ferris M. J., and, Jones S. R., (2014) Biphasic mechanisms of amphetamine action at the dopamine terminal. J. Neurosci. 34, 5575-5582.
29. Smolders I., Klippel N., De Sarre. S., Ebinger G., and, Michotte Y., (1995) Tonic GABA-ergic modulation of striatal dopamine release studied by in vivo microdialysis in the freely moving rat. Eur. J. Pharmacol. 284, 83-91.
30. Stamatakis A. M., Jennings J. H., Ung R. L., Blair G. A., Weinberg R. J., Neve R. L., Boyce F., et al,. (2013) A unique population of ventral tegmental area neurons inhibits the lateral habenula to promote reward. Neuron 80, 1039-1053.
31. Stuber G. D., Hnasko T. S., Britt J. P., Edwards R. H., and, Bonci A., (2010) Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. J. Neurosci. 30, 8229-8233.
32. Stuber G. D., Britt J. P., and, Bonci A., (2012) Optogenetic modulation of neural circuits that underlie reward seeking. Biol. Psychiatry 71, 1061-1067.
33. Tecuapetla F., Patel J. C., Xenias H., et al,. (2010) Glutamatergic signaling by mesolimbic dopamine neurons in the nucleus accumbens. J. Neurosci. 30, 7105-7110.
34. Tepper J. M., and, Bolam J. P., (2004) Functional diversity and specificity of neostriatal interneurons. Curr. Opin. Neurobiol. 14, 685-692.
35. Tepper J. M., Tecuapetla F., Koõs T., and, Ibáñez-Sandoval O., (2010) Heterogeneity and diversity of striatal GABAergic interneurons. Front. Neuroanat. 4, 150.
36. Threlfell S., Clements M. A., Khodai T., Pienaar I. S., Exley R., Wess J., and, Cragg S. J., (2010) Striatal muscarinic receptors promote activity dependence of dopamine transmission via distinct receptor subtypes on cholinergic interneurons in ventral versus dorsal striatum. J. Neurosci. 30, 3398-3408.
37. Threlfell S., Lalic T., Platt N. J., Jennings K. A., Deisseroth K., and, Cragg S. J., (2012) Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 75, 58-64.
38. Tritsch N. X., Ding J. B., and, Sabatini B. L., (2012) Dopaminergic neurons inhibit striatal output through non-canonical release of GABA. Nature 490, 262-266.
39. Tritsch N. X., Oh W.-J., Gu C., and, Sabatini B. L., (2014) Midbrain dopamine neurons sustain inhibitory transmission using plasma membrane uptake of GABA, not synthesis. ELife 3, e01936.
40. Tsai H.-C., Zhang F., Adamantidis A., Stuber G. D., Bonci A., de Lecea L., and, Deisseroth K., (2009) Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324, 1080-1084.
41. Tye K. M., Mirzabekov J. J., Warden M. R., et al,. (2013) Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 493, 537-541.
42. Wang L., Zhang X., Xu H., et al,. (2014) Temporal components of cholinergic terminal to dopaminergic terminal transmission in dorsal striatum slices of mice. J. Physiol. 592, 3559-3576.
43. Wightman R. M., Amatore C., Engstrom R. C., Hale P. D., Kristensen E. W., Kuhr W. G., and, May L. J., (1988) Real-time characterization of dopamine overflow and uptake in the rat striatum. Neuroscience 25, 513-523.
44. Witten I. B., Steinberg E. E., Lee S. Y., et al,. (2011) Recombinase-driver rat lines: tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron 72, 721-733.
45. Yorgason J. T., España R. A., and, Jones S. R., (2011) Demon voltammetry and analysis software: analysis of cocaine-induced alterations in dopamine signaling using multiple kinetic measures. J. Neurosci. Methods 202, 158-164.
46. Yorgason J. T., Ferris M. J., Steffensen S. C., and, Jones S. R., (2014) Frequency-dependent effects of ethanol on dopamine release in the nucleus accumbens. Alcohol. Clin. Exp. Res. 38, 438-447.
47. Zhang H., and, Sulzer D., (2003) Glutamate spillover in the striatum depresses dopaminergic transmission by activating group I metabotropic glutamate receptors. J. Neurosci. 23, 10585-10592.
48. Zhang H., and, Sulzer D., (2004) Frequency-dependent modulation of dopamine release by nicotine. Nat. Neurosci. 7, 581-582.
49. Zhang L., Doyon W. M., Clark J. J., Phillips P. E. M., and, Dani J. A., (2009) Controls of tonic and phasic dopamine transmission in the dorsal and ventral striatum. Mol. Pharmacol. 76, 396-404.
50. Zhou F. M., Liang Y., and, Dani J. A., (2001) Endogenous nicotinic cholinergic activity regulates dopamine release in the striatum. Nat. Neurosci. 4, 1224-1229.