Distinct sub-second dopamine signaling in dorsolateral striatum measured by a genetically-encoded fluorescent sensor.

Armando G Salinas, Jeong Oen Lee, Shana M Augustin, Shiliang Zhang, Tommaso Patriarchi, Lin Tian, Marisela Morales, Yolanda Mateo, David M Lovinger
Author Information
  1. Armando G Salinas: Laboratory for Integrative Neuroscience, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Rockville, MD, USA. armando.salinas@lsuhs.edu. ORCID
  2. Jeong Oen Lee: Laboratory for Integrative Neuroscience, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Rockville, MD, USA.
  3. Shana M Augustin: Laboratory for Integrative Neuroscience, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Rockville, MD, USA.
  4. Shiliang Zhang: Confocal and Electron Microscopy Core, National Institute on Drug Abuse, Baltimore, MD, USA. ORCID
  5. Tommaso Patriarchi: Department of Biochemistry and Molecular Medicine, University of California at Davis, Davis, CA, USA. ORCID
  6. Lin Tian: Department of Biochemistry and Molecular Medicine, University of California at Davis, Davis, CA, USA. ORCID
  7. Marisela Morales: Neuronal Networks Section, Integrative Neuroscience Research Branch, National Institute on Drug Abuse, Baltimore, MD, USA. ORCID
  8. Yolanda Mateo: Laboratory for Integrative Neuroscience, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Rockville, MD, USA.
  9. David M Lovinger: Laboratory for Integrative Neuroscience, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Rockville, MD, USA. lovindav@mail.nih.gov. ORCID

Abstract

The development of genetically encoded dopamine sensors such as dLight has provided a new approach to measuring slow and fast dopamine dynamics both in brain slices and in vivo, possibly enabling dopamine measurements in areas like the dorsolateral striatum (DLS) where previously such recordings with fast-scan cyclic voltammetry (FSCV) were difficult. To test this, we first evaluated dLight photometry in mouse brain slices with simultaneous FSCV and found that both techniques yielded comparable results, but notable differences in responses to dopamine transporter inhibitors, including cocaine. We then used in vivo fiber photometry with dLight in mice to examine responses to cocaine in DLS. We also compared dopamine responses during Pavlovian conditioning across the striatum. We show that dopamine increases were readily detectable in DLS and describe transient dopamine kinetics, as well as slowly developing signals during conditioning. Overall, our findings indicate that dLight photometry is well suited to measuring dopamine dynamics in DLS.

References

  1. Front Pharmacol. 2019 Feb 14;10:72 [PMID: 30837868]
  2. J Neurosci Methods. 2011 Nov 15;202(2):158-64 [PMID: 21392532]
  3. Neuron. 2020 Oct 14;108(1):17-32 [PMID: 33058762]
  4. Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):4029-34 [PMID: 9520487]
  5. Elife. 2021 Oct 05;10: [PMID: 34608866]
  6. J Neurosci. 2004 Feb 11;24(6):1265-71 [PMID: 14960596]
  7. Trends Neurosci. 2014 Apr;37(4):200-10 [PMID: 24656971]
  8. Sci Rep. 2019 Mar 19;9(1):4857 [PMID: 30890737]
  9. Nat Neurosci. 2018 Jun;21(6):787-793 [PMID: 29760524]
  10. Mol Pharmacol. 2000 Jul;58(1):109-19 [PMID: 10860932]
  11. Neuron. 2014 Oct 1;84(1):164-176 [PMID: 25242218]
  12. Neurosci Lett. 2009 Dec 25;467(2):144-6 [PMID: 19822192]
  13. Curr Biol. 2022 Mar 14;32(5):1163-1174.e6 [PMID: 35134325]
  14. Biol Psychiatry. 2006 Jun 15;59(12):1151-9 [PMID: 16566899]
  15. Nat Protoc. 2014;9(6):1213-28 [PMID: 24784819]
  16. Cell Rep. 2012 Jul 26;2(1):33-41 [PMID: 22840394]
  17. Trends Cogn Sci. 2019 Mar;23(3):213-234 [PMID: 30711326]
  18. Nat Neurosci. 2001 Dec;4(12):1224-9 [PMID: 11713470]
  19. J Neurosci Methods. 2004 Dec 30;140(1-2):183-7 [PMID: 15589348]
  20. Trends Neurosci. 2004 May;27(5):270-7 [PMID: 15111009]
  21. Front Neural Circuits. 2016 Dec 20;10:105 [PMID: 28066191]
  22. Curr Opin Neurobiol. 2018 Feb;48:9-16 [PMID: 28843800]
  23. Neuron. 2012 Jul 12;75(1):58-64 [PMID: 22794260]
  24. Neuropsychopharmacology. 2018 Sep;43(10):2083-2092 [PMID: 29795245]
  25. Neuropsychopharmacology. 2021 Jul;46(8):1432-1441 [PMID: 33452430]
  26. Front Behav Neurosci. 2010 Nov 04;4:170 [PMID: 21120145]
  27. Learn Mem. 2004 Jul-Aug;11(4):459-63 [PMID: 15286184]
  28. Neuron. 2017 Oct 11;96(2):476-489.e5 [PMID: 29024667]
  29. Nature. 1996 Feb 15;379(6566):606-12 [PMID: 8628395]
  30. Neuropharmacology. 2016 Sep;108:275-83 [PMID: 27036891]
  31. Cell. 2018 Jul 12;174(2):481-496.e19 [PMID: 30007419]
  32. PLoS One. 2014 Oct 31;9(10):e111749 [PMID: 25360513]
  33. Analyst. 2003 Dec;128(12):1413-9 [PMID: 14737224]
  34. J Neurosci. 2006 Mar 22;26(12):3206-9 [PMID: 16554471]
  35. Elife. 2021 Mar 10;10: [PMID: 33689680]
  36. Neuroscience. 2002;114(2):475-92 [PMID: 12204216]
  37. Proc Natl Acad Sci U S A. 2023 Feb 14;120(7):e2215230120 [PMID: 36749722]
  38. Nat Rev Neurosci. 2021 Jun;22(6):345-358 [PMID: 33837376]
  39. J Neurosci. 2002 May 15;22(10):RC222 [PMID: 12006604]
  40. Proc Natl Acad Sci U S A. 2012 Dec 11;109(50):20703-8 [PMID: 23184975]
  41. Cell Rep. 2021 Aug 3;36(5):109465 [PMID: 34348146]
  42. J Neurochem. 2003 Dec;87(5):1284-95 [PMID: 14622108]
  43. Nat Methods. 2016 Apr;13(4):325-8 [PMID: 26878381]
  44. ACS Chem Neurosci. 2015 Nov 18;6(11):1802-12 [PMID: 26322962]
  45. Neurochem Int. 2012 Dec;61(7):986-91 [PMID: 22819794]
  46. Nature. 2013 Aug 29;500(7464):575-9 [PMID: 23913271]
  47. Neuroscience. 2017 Mar 14;345:110-123 [PMID: 27185487]
  48. Sci Rep. 2016 Nov 25;6:37834 [PMID: 27886263]
  49. Nature. 2019 Jun;570(7759):65-70 [PMID: 31118513]
  50. J Physiol. 2015 May 15;593(10):2295-310 [PMID: 25781000]
  51. Curr Protoc Neurosci. 2009 Apr;Chapter 7:Unit7.1 [PMID: 19340812]
  52. ACS Chem Neurosci. 2016 Jun 15;7(6):700-9 [PMID: 27018734]
  53. J Neurosci. 2009 Oct 21;29(42):13344-52 [PMID: 19846722]
  54. Nature. 2023 Feb;614(7946):108-117 [PMID: 36653449]
  55. Nat Neurosci. 2015 Mar;18(3):386-92 [PMID: 25664911]
  56. Nat Rev Neurosci. 2016 Aug;17(8):524-32 [PMID: 27256556]
  57. Analyst. 2020 Feb 17;145(4):1158-1168 [PMID: 31922176]
  58. Int J Mol Sci. 2020 Oct 28;21(21): [PMID: 33126757]
  59. Nat Neurosci. 2016 Jan;19(1):117-26 [PMID: 26595651]
  60. Science. 2018 Jun 29;360(6396): [PMID: 29853555]
  61. J Neurochem. 1988 Oct;51(4):1314-6 [PMID: 3418351]
  62. J Neurosci. 2001 Aug 15;21(16):6338-47 [PMID: 11487657]
  63. Curr Opin Neurobiol. 2014 Dec;29:109-17 [PMID: 25058111]
  64. Science. 1997 Mar 14;275(5306):1593-9 [PMID: 9054347]
  65. Front Synaptic Neurosci. 2014 Sep 04;6:19 [PMID: 25237305]
  66. Front Cell Neurosci. 2019 Feb 12;13:32 [PMID: 30809128]
  67. Nat Neurosci. 2007 Aug;10(8):1020-8 [PMID: 17603481]
  68. Brain. 2009 Feb;132(Pt 2):285-7 [PMID: 19168452]
  69. Eur J Pharmacol. 1987 Jul 23;139(3):345-8 [PMID: 3666010]
  70. Neuroscience. 1994 Mar;59(2):417-27 [PMID: 8008199]
  71. Acta Pharmacol Sin. 2020 Feb;41(2):163-172 [PMID: 31399700]
  72. Nature. 2013 Feb 14;494(7436):238-42 [PMID: 23354054]
  73. Eur J Neurosci. 2011 Dec;34(12):1997-2006 [PMID: 22122410]
  74. J Neurosci. 2010 Jul 21;30(29):9762-70 [PMID: 20660258]

Grants

  1. ZIA AA000407/Intramural NIH HHS
  2. K99 AA025991/NIAAA NIH HHS
  3. R00 AA025991/NIAAA NIH HHS
  4. DP2 MH107056/NIMH NIH HHS
  5. U01 NS090604/NINDS NIH HHS
  6. R00 AA027740/NIAAA NIH HHS

MeSH Term

Animals
Mice
Dopamine
Corpus Striatum
Neostriatum
Brain
Cocaine
Coloring Agents

Chemicals

Dopamine
Cocaine
Coloring Agents

Word Cloud

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