Synaptotagmin-1-dependent phasic axonal dopamine release is dispensable for basic motor behaviors in mice.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
11 07 2023
11 07 2023
Historique:
received:
18
10
2021
accepted:
27
06
2023
medline:
13
7
2023
pubmed:
12
7
2023
entrez:
11
7
2023
Statut:
epublish
Résumé
In Parkinson's disease (PD), motor dysfunctions only become apparent after extensive loss of DA innervation. This resilience has been hypothesized to be due to the ability of many motor behaviors to be sustained through a diffuse basal tone of DA; but experimental evidence for this is limited. Here we show that conditional deletion of the calcium sensor synaptotagmin-1 (Syt1) in DA neurons (Syt1 cKO
Identifiants
pubmed: 37433762
doi: 10.1038/s41467-023-39805-7
pii: 10.1038/s41467-023-39805-7
pmc: PMC10336101
doi:
Substances chimiques
Caffeine
3G6A5W338E
Calcium
SY7Q814VUP
Dopamine
VTD58H1Z2X
Niacinamide
25X51I8RD4
Syt1 protein, mouse
0
Synaptotagmin I
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4120Informations de copyright
© 2023. The Author(s).
Références
Schultz, W. Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 30, 259–288 (2007).
pubmed: 17600522
doi: 10.1146/annurev.neuro.28.061604.135722
Surmeier, D. J., Graves, S. M. & Shen, W. Dopaminergic modulation of striatal networks in health and Parkinson’s disease. Curr. Opin. Neurobiol. 29, 109–117 (2014).
pubmed: 25058111
pmcid: 4418190
doi: 10.1016/j.conb.2014.07.008
Hauber, W. Impairments of movement initiation and execution induced by a blockade of dopamine D1 or D2 receptors are reversed by a blockade of N-methyl-D-aspartate receptors. Neuroscience 73, 121–130 (1996).
pubmed: 8783236
doi: 10.1016/0306-4522(96)00036-X
Mercuri, N. B. & Bernardi, G. The ‘magic’ of l-dopa: why is it the gold standard Parkinson’s disease therapy? Trends Pharmacol. Sci. 26, 341–344 (2005).
pubmed: 15936832
doi: 10.1016/j.tips.2005.05.002
Golden, J. P. et al. Dopamine-dependent compensation maintains motor behavior in mice with developmental ablation of dopaminergic neurons. J. Neurosci. 33, 17095–17107 (2013).
pubmed: 24155314
pmcid: 3807031
doi: 10.1523/JNEUROSCI.0890-13.2013
Descarries, L., Watkins, K. C., Garcia, S., Bosler, O. & Doucet, G. Dual character, asynaptic and synaptic, of the dopamine innervation in adult rat neostriatum: a quantitative autoradiographic and immunocytochemical analysis. J. Comp. Neurol. 375, 167–186 (1996).
pubmed: 8915824
doi: 10.1002/(SICI)1096-9861(19961111)375:2<167::AID-CNE1>3.0.CO;2-0
Antonopoulos, J., Dori, I., Dinopoulos, A., Chiotelli, M. & Parnavelas, J. G. Postnatal development of the dopaminergic system of the striatum in the rat. Neuroscience 110, 245–256 (2002).
pubmed: 11958867
doi: 10.1016/S0306-4522(01)00575-9
Descarries, L. et al. Glutamate in dopamine neurons: Synaptic versus diffuse transmission. Brain Res. Rev. 58, 290–302 (2008).
pubmed: 18042492
doi: 10.1016/j.brainresrev.2007.10.005
Ducrot, C. et al. Dopaminergic neurons establish a distinctive axonal arbor with a majority of non-synaptic terminals. FASEB J. 35, e21791 (2021).
pubmed: 34320240
doi: 10.1096/fj.202100201RR
Rice, M. E. & Patel, J. C. Somatodendritic dopamine release: recent mechanistic insights. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 370, 20140185 (2015).
Mendez, J. A., Bourque, M.-J., Fasano, C., Kortleven, C. & Trudeau, L.-E. Somatodendritic dopamine release requires synaptotagmin 4 and 7 and the participation of voltage-gated calcium channels. J. Biol. Chem. 286, 23928–23937 (2011).
pubmed: 21576241
pmcid: 3129174
doi: 10.1074/jbc.M111.218032
Liu, C., Kershberg, L., Wang, J., Schneeberger, S. & Kaeser, P. S. Dopamine secretion is mediated by sparse active zone-like release sites. Cell 172, 706–718.e15 (2018).
pubmed: 29398114
pmcid: 5807134
doi: 10.1016/j.cell.2018.01.008
Banerjee, A. et al. Molecular and functional architecture of striatal dopamine release sites. Neuron 110, 248–265.e9 (2022).
Liu, C., Goel, P. & Kaeser, P. S. Spatial and temporal scales of dopamine transmission. Nat. Rev. Neurosci. 1–14 https://doi.org/10.1038/s41583-021-00455-7 (2021).
Fortin, G. D., Desrosiers, C. C., Yamaguchi, N. & Trudeau, L. E. Basal somatodendritic dopamine release requires snare proteins. J. Neurochem. 96, 1740–1749 (2006).
pubmed: 16539689
doi: 10.1111/j.1471-4159.2006.03699.x
Bergquist, F., Niazi, H. S. & Nissbrandt, H. Evidence for different exocytosis pathways in dendritic and terminal dopamine release in vivo. Brain Res. 950, 245–253 (2002).
pubmed: 12231250
doi: 10.1016/S0006-8993(02)03047-0
Ovsepian, S. V. & Dolly, J. O. Dendritic SNAREs add a new twist to the old neuron theory. Proc. Natl Acad. Sci. USA 108, 19113–19120 (2011).
pubmed: 22080607
pmcid: 3228427
doi: 10.1073/pnas.1017235108
Hikima, T. et al. Activity-dependent somatodendritic dopamine release in the substantia nigra autoinhibits the releasing neuron. Cell Rep. 35, 108951 (2021).
pubmed: 33826884
pmcid: 8189326
doi: 10.1016/j.celrep.2021.108951
Sudhof, T. C. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509–547 (2004).
pubmed: 15217342
doi: 10.1146/annurev.neuro.26.041002.131412
Andrews, N. W. & Chakrabarti, S. There’s more to life than neurotransmission: the regulation of exocytosis by synaptotagmin VII. Trends Cell Biol. 15, 626–631 (2005).
pubmed: 16168654
doi: 10.1016/j.tcb.2005.09.001
Xu, J., Mashimo, T. & Südhof, T. C. Synaptotagmin-1, −2, and −9: Ca(2+) sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron 54, 567–581 (2007).
pubmed: 17521570
doi: 10.1016/j.neuron.2007.05.004
Banerjee, A., Lee, J., Nemcova, P., Liu, C. & Kaeser, P. S. Synaptotagmin-1 is the Ca2+ sensor for fast striatal dopamine release. eLife 9, e58359 (2020).
pubmed: 32490813
pmcid: 7319770
doi: 10.7554/eLife.58359
Delignat-Lavaud, B., Ducrot, C., Kouwenhoven, W., Feller, N. & Trudeau, L.-É. Implication of synaptotagmins 4 and 7 in activity-dependent somatodendritic dopamine release in the ventral midbrain. Open Biol. 12, 210339 (2022).
Hikima, T., Witkovsky, P., Khatri, L., Chao, M. V. & Rice, M. E. Synaptotagmins 1 and 7 play complementary roles in somatodendritic dopamine release. J. Neurosci. 42, 3919–3930 (2022).
pubmed: 35361702
pmcid: 9097777
doi: 10.1523/JNEUROSCI.2416-21.2022
Lebowitz, J. J. et al. Synaptotagmin-1 is a Ca
pubmed: 36640316
doi: 10.1016/j.celrep.2022.111915
Robinson, B. G. et al. RIM is essential for stimulated but not spontaneous somatodendritic dopamine release in the midbrain. eLife 8, e47972 (2019).
pubmed: 31486769
pmcid: 6754207
doi: 10.7554/eLife.47972
Deutch, A. Y., Goldstein, M., Baldino, F. & Roth, R. H. Telencephalic projections of the A8 dopamine cell group. Ann. N. Y. Acad. Sci. 537, 27–50 (1988).
pubmed: 2462395
doi: 10.1111/j.1749-6632.1988.tb42095.x
Bayer, V. E. & Pickel, V. M. Ultrastructural localization of tyrosine hydroxylase in the rat ventral tegmental area: relationship between immunolabeling density and neuronal associations. J. Neurosci. 10, 2996–3013 (1990).
pubmed: 1975839
pmcid: 6570237
doi: 10.1523/JNEUROSCI.10-09-02996.1990
Juraska, J. M., Wilson, C. J. & Groves, P. M. The substantia nigra of the rat: a Golgi study. J. Comp. Neurol. 172, 585–600 (1977).
pubmed: 65369
doi: 10.1002/cne.901720403
Wassef, M., Berod, A. & Sotelo, C. Dopaminergic dendrites in the pars reticulata of the rat substantia nigra and their striatal input. combined immunocytochemical localization of tyrosine hydroxylase and anterograde degeneration. Neuroscience 6, 2125–2139 (1981).
pubmed: 6120482
doi: 10.1016/0306-4522(81)90003-8
Matsuda, W. et al. Single nigrostriatal dopaminergic neurons form widely spread and highly dense axonal arborizations in the neostriatum. J. Neurosci. 29, 444–453 (2009).
pubmed: 19144844
pmcid: 6664950
doi: 10.1523/JNEUROSCI.4029-08.2009
Lim, S. T., Antonucci, D. E., Scannevin, R. H. & Trimmer, J. S. A novel targeting signal for proximal clustering of the Kv2.1 K+ channel in hippocampal neurons. Neuron 25, 385–397 (2000).
pubmed: 10719893
doi: 10.1016/S0896-6273(00)80902-2
Misonou, H., Mohapatra, D. P. & Trimmer, J. S. Kv2.1: a voltage-gated K+ channel critical to dynamic control of neuronal excitability. NeuroToxicology 26, 743–752 (2005).
pubmed: 15950285
doi: 10.1016/j.neuro.2005.02.003
Jensen, C. S. et al. Trafficking of Kv2.1 channels to the axon initial segment by a novel nonconventional secretory pathway. J. Neurosci. 37, 11523–11536 (2017).
pubmed: 29042434
pmcid: 6705746
doi: 10.1523/JNEUROSCI.3510-16.2017
Baker, C. A., Elyada, Y. M., Parra, A. & Bolton, M. M. Cellular resolution circuit mapping with temporal-focused excitation of soma-targeted channelrhodopsin. eLife 5, e14193 (2016).
O’Neill, B., Patel, J. C. & Rice, M. E. Characterization of optically and electrically evoked dopamine release in striatal slices from digenic knock-in mice with DAT-driven expression of channelrhodopsin. ACS Chem. Neurosci. 8, 310–319 (2017).
pubmed: 28177213
doi: 10.1021/acschemneuro.6b00300
Bergquist, F., Shahabi, H. N. & Nissbrandt, H. Somatodendritic dopamine release in rat substantia nigra influences motor performance on the accelerating rod. Brain Res. 973, 81–91 (2003).
pubmed: 12729956
doi: 10.1016/S0006-8993(03)02555-1
Joshua, M., Adler, A. & Bergman, H. The dynamics of dopamine in control of motor behavior. Curr. Opin. Neurobiol. 19, 615–620 (2009).
pubmed: 19896833
doi: 10.1016/j.conb.2009.10.001
Halliday, G. M. et al. Neuropathology of immunohistochemically identified brainstem neurons in Parkinson’s disease. Ann. Neurol. 27, 373–385 (1990).
pubmed: 1972319
doi: 10.1002/ana.410270405
Ward, K. M. & Citrome, L. Antipsychotic-related movement disorders: drug-induced parkinsonism vs. tardive dyskinesia—key differences in pathophysiology and clinical management. Neurol. Ther. 7, 233–248 (2018).
pubmed: 30027457
pmcid: 6283785
doi: 10.1007/s40120-018-0105-0
Matikainen-Ankney, B. A. et al. An open-source device for measuring food intake and operant behavior in rodent home-cages. eLife 10, e66173 (2021).
pubmed: 33779547
pmcid: 8075584
doi: 10.7554/eLife.66173
Bauman, R. An experimental analysis of the cost of food in a closed economy. J. Exp. Anal. Behav. 56, 33–50 (1991).
pubmed: 1940762
pmcid: 1323081
doi: 10.1901/jeab.1991.56-33
Chaney, M. A. & Rowland, N. E. Food demand functions in mice. Appetite 51, 669–675 (2008).
pubmed: 18590781
pmcid: 2570480
doi: 10.1016/j.appet.2008.06.002
Beeler, J. A., Daw, N., Frazier, C. R. M. & Zhuang, X. Tonic dopamine modulates exploitation of reward learning. Front. Behav. Neurosci. 4, 170 (2010).
pubmed: 21120145
pmcid: 2991243
doi: 10.3389/fnbeh.2010.00170
Mourra, D., Gnazzo, F., Cobos, S. & Beeler, J. A. Striatal dopamine D2 receptors regulate cost sensitivity and behavioral thrift. Neuroscience 425, 134–145 (2020).
pubmed: 31809732
doi: 10.1016/j.neuroscience.2019.11.002
Donnan, G. A. et al. Evidence for plasticity of the dopaminergic system in Parkinsonism. Mol. Neurobiol. 5, 421–433 (1991).
pubmed: 1823144
doi: 10.1007/BF02935563
Richard, M. G. & Bennett, J. P. Regulation by D2 dopamine receptors of in vivo dopamine synthesis in striata of rats and mice with experimental parkinsonism. Exp. Neurol. 129, 57–63 (1994).
pubmed: 7925842
doi: 10.1006/exnr.1994.1146
Stamford, J. A., Kruk, Z. L. & Millar, J. Actions of dopamine antagonists on stimulated striatal and limbic dopamine release: an in vivo voltammetric study. Br. J. Pharm. 94, 924–932 (1988).
doi: 10.1111/j.1476-5381.1988.tb11605.x
Palij, P. et al. Presynaptic regulation of dopamine release in corpus striatum monitored in vitro in real time by fast cyclic voltammetry. Brain Res 509, 172–174 (1990).
pubmed: 2137719
doi: 10.1016/0006-8993(90)90329-A
Fawaz, C. S., Martel, P., Leo, D. & Trudeau, L.-E. Presynaptic action of neurotensin on dopamine release through inhibition of D2 receptor function. BMC Neurosci. 10, 96 (2009).
pubmed: 19682375
pmcid: 2745416
doi: 10.1186/1471-2202-10-96
Hoffman, A. F., Spivak, C. E. & Lupica, C. R. Enhanced dopamine release by dopamine transport inhibitors described by a restricted diffusion model and fast-scan cyclic voltammetry. ACS Chem. Neurosci. 7, 700–709 (2016).
pubmed: 27018734
doi: 10.1021/acschemneuro.5b00277
Carvelli, L., McDonald, P. W., Blakely, R. D. & DeFelice, L. J. Dopamine transporters depolarize neurons by a channel mechanism. Proc. Natl Acad. Sci. USA 101, 16046–16051 (2004).
pubmed: 15520385
pmcid: 528740
doi: 10.1073/pnas.0403299101
Sun, W., Ginovart, N., Ko, F., Seeman, P. & Kapur, S. In vivo evidence for dopamine-mediated internalization of D2-receptors after amphetamine: differential findings with [3H]raclopride versus [3H]spiperone. Mol. Pharm. 63, 456–462 (2003).
doi: 10.1124/mol.63.2.456
Guo, N. et al. Impact of D2 receptor internalization on binding affinity of neuroimaging radiotracers. Neuropsychopharmacology 35, 806–817 (2010).
pubmed: 19956086
doi: 10.1038/npp.2009.189
Parish, C. L., Finkelstein, D. I., Drago, J., Borrelli, E. & Horne, M. K. The role of dopamine receptors in regulating the size of axonal arbors. J. Neurosci. 21, 5147–5157 (2001).
pubmed: 11438590
pmcid: 6762846
doi: 10.1523/JNEUROSCI.21-14-05147.2001
Tripanichkul, W., Stanic, D., Drago, J., Finkelstein, D. I. & Horne, M. K. D2 dopamine receptor blockade results in sprouting of DA axons in the intact animal but prevents sprouting following nigral lesions. Eur. J. Neurosci. 17, 1033–1045 (2003).
pubmed: 12653979
doi: 10.1046/j.1460-9568.2003.02547.x
Fasano, C., Poirier, A., DesGroseillers, L. & Trudeau, L.-E. Chronic activation of the D2 dopamine autoreceptor inhibits synaptogenesis in mesencephalic dopaminergic neurons in vitro. Eur. J. Neurosci. 28, 1480–1490 (2008).
pubmed: 18973573
doi: 10.1111/j.1460-9568.2008.06450.x
Fasano, C., Kortleven, C. & Trudeau, L.-E. Chronic activation of the D2 autoreceptor inhibits both glutamate and dopamine synapse formation and alters the intrinsic properties of mesencephalic dopamine neurons in vitro. Eur. J. Neurosci. 32, 1433–1441 (2010).
pubmed: 20846243
doi: 10.1111/j.1460-9568.2010.07397.x
Fasano, C. et al. Dopamine facilitates dendritic spine formation by cultured striatal medium spiny neurons through both D1 and D2 dopamine receptors. Neuropharmacology 67, 432–443 (2013).
pubmed: 23231809
doi: 10.1016/j.neuropharm.2012.11.030
Giguère, N. et al. Increased vulnerability of nigral dopamine neurons after expansion of their axonal arborization size through D2 dopamine receptor conditional knockout. PLoS Genet. 15, e1008352 (2019).
pubmed: 31449520
pmcid: 6730950
doi: 10.1371/journal.pgen.1008352
Gagnon, D. et al. Evidence for sprouting of dopamine and serotonin axons in the pallidum of Parkinsonian monkeys. Front. Neuroanat. 12, 38 (2018).
Maximov, A. et al. Genetic analysis of synaptotagmin-7 function in synaptic vesicle exocytosis. Proc. Natl Acad. Sci. USA 105, 3986–3991 (2008).
pubmed: 18308933
pmcid: 2268828
doi: 10.1073/pnas.0712372105
Bacaj, T. et al. Synaptotagmin-1 and synaptotagmin-7 trigger synchronous and asynchronous phases of neurotransmitter release. Neuron 80, 947–959 (2013).
pubmed: 24267651
pmcid: 3888870
doi: 10.1016/j.neuron.2013.10.026
Bacaj, T. et al. Synaptotagmin-1 and −7 are redundantly essential for maintaining the capacity of the readily-releasable pool of synaptic vesicles. PLoS Biol. 13, e1002267 (2015).
pubmed: 26437117
pmcid: 4593569
doi: 10.1371/journal.pbio.1002267
Wang, C. et al. Synaptotagmin-11 is a critical mediator of parkin-linked neurotoxicity and Parkinson’s disease-like pathology. Nat. Commun. 9, 1–14 (2018).
Pang, Z. P. et al. Doc2 supports spontaneous synaptic transmission by a Ca2+-independent mechanism. Neuron 70, 244–251 (2011).
pubmed: 21521611
pmcid: 3102832
doi: 10.1016/j.neuron.2011.03.011
Sulzer, D., Cragg, S. J. & Rice, M. E. Striatal dopamine neurotransmission: regulation of release and uptake. Basal Ganglia 6, 123–148 (2016).
pubmed: 27141430
pmcid: 4850498
doi: 10.1016/j.baga.2016.02.001
Sulzer, D., Sonders, M. S., Poulsen, N. W. & Galli, A. Mechanisms of neurotransmitter release by amphetamines: a review. Prog. Neurobiol. 75, 406–433 (2005).
pubmed: 15955613
doi: 10.1016/j.pneurobio.2005.04.003
Parish, C. L. et al. Effects of long-term treatment with dopamine receptor agonists and antagonists on terminal arbor size. Eur. J. Neurosci. 16, 787–794 (2002).
pubmed: 12372014
doi: 10.1046/j.1460-9568.2002.02132.x
Chen, B. T., Patel, J. C., Moran, K. A. & Rice, M. E. Differential calcium dependence of axonal versus somatodendritic dopamine release, with characteristics of both in the ventral tegmental area. Front. Syst. Neurosci. 5, 39 (2011).
pubmed: 21716634
pmcid: 3115476
doi: 10.3389/fnsys.2011.00039
Beckstead, M. J., Grandy, D. K., Wickman, K. & Williams, J. T. Vesicular dopamine release elicits an inhibitory postsynaptic current in midbrain dopamine neurons. Neuron 42, 939–946 (2004).
pubmed: 15207238
doi: 10.1016/j.neuron.2004.05.019
Beckstead, M. J., Ford, C. P., Phillips, P. E. M. & Williams, J. T. Presynaptic regulation of dendrodendritic dopamine transmission. Eur. J. Neurosci. 26, 1479–1488 (2007).
pubmed: 17822435
pmcid: 3633601
doi: 10.1111/j.1460-9568.2007.05775.x
Courtney, N. A., Mamaligas, A. A. & Ford, C. P. Species differences in somatodendritic dopamine transmission determine D2-autoreceptor-mediated inhibition of ventral tegmental area neuron firing. J. Neurosci. 32, 13520–13528 (2012).
pubmed: 23015441
pmcid: 3538874
doi: 10.1523/JNEUROSCI.2745-12.2012
Ford, C. P., Phillips, P. E. M. & Williams, J. T. The time course of dopamine transmission in the ventral tegmental area. J. Neurosci. 29, 13344–13352 (2009).
pubmed: 19846722
pmcid: 2791792
doi: 10.1523/JNEUROSCI.3546-09.2009
Ford, C. P., Gantz, S. C., Phillips, P. E. M. & Williams, J. T. Control of extracellular dopamine at dendrite and axon terminals. J. Neurosci. 30, 6975–6983 (2010).
pubmed: 20484639
pmcid: 2883253
doi: 10.1523/JNEUROSCI.1020-10.2010
Fernandes Xavier, F. G., Doucet, G., Geffard, M. & Descarries, L. Dopamine neoinnervation in the substantia nigra and hyperinnervation in the interpeduncular nucleus of adult rat following neonatal cerebroventricular administration of 6-hydroxydopamine. Neuroscience 59, 77–87 (1994).
pubmed: 8190274
doi: 10.1016/0306-4522(94)90100-7
Bezard, E., Gross, C. E. & Brotchie, J. M. Presymptomatic compensation in Parkinson’s disease is not dopamine-mediated. Trends Neurosci. 26, 215–221 (2003).
pubmed: 12689773
doi: 10.1016/S0166-2236(03)00038-9
Parmar, M., Torper, O. & Drouin-Ouellet, J. Cell-based therapy for Parkinson’s disease: a journey through decades toward the light side of the force. Eur. J. Neurosci. 49, 463–471 (2019).
pubmed: 30099795
doi: 10.1111/ejn.14109
Palmiter, R. D. Dopamine signaling in the dorsal striatum is essential for motivated behaviors: lessons from dopamine-deficient mice. Ann. N. Y Acad. Sci. 1129, 35–46 (2008).
pubmed: 18591467
pmcid: 2720267
doi: 10.1196/annals.1417.003
Cagniard, B. et al. Dopamine scales performance in the absence of new learning. Neuron 51, 541–547 (2006).
pubmed: 16950153
doi: 10.1016/j.neuron.2006.07.026
Berridge, K. C. The debate over dopamine’s role in reward: the case for incentive salience. Psychopharmacology 191, 391–431 (2007).
pubmed: 17072591
doi: 10.1007/s00213-006-0578-x
Ferris, M. J. et al. Dopamine transporters govern diurnal variation in extracellular dopamine tone. Proc. Natl Acad. Sci. USA 111, E2751–E2759 (2014).
pubmed: 24979798
pmcid: 4084435
doi: 10.1073/pnas.1407935111
Zweifel, L. S. et al. Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior. Proc. Natl Acad. Sci. USA 106, 7281–7288 (2009).
pubmed: 19342487
pmcid: 2678650
doi: 10.1073/pnas.0813415106
Kochubey, O., Babai, N. & Schneggenburger, R. A synaptotagmin isoform switch during the development of an identified CNS synapse. Neuron 90, 984–999 (2016).
pubmed: 27210552
doi: 10.1016/j.neuron.2016.04.038
Rice, M. E. et al. Direct monitoring of dopamine and 5-HT release in substantia nigra and ventral tegmental area in vitro. Exp. Brain Res 100, 395–406 (1994).
pubmed: 7813678
doi: 10.1007/BF02738400
Cragg, S. J., Hawkey, C. R. & Greenfield, S. A. Comparison of serotonin and dopamine release in substantia nigra and ventral tegmental area: region and species differences. J. Neurochem. 69, 2378–2386 (1997).
pubmed: 9375669
doi: 10.1046/j.1471-4159.1997.69062378.x
Itzhak, Y. & Martin, J. L. Effects of cocaine, nicotine, dizocipline and alcohol on mice locomotor activity: cocaine–alcohol cross-sensitization involves upregulation of striatal dopamine transporter binding sites. Brain Res. 818, 204–211 (1999).
pubmed: 10082805
doi: 10.1016/S0006-8993(98)01260-8
Steinkellner, T. et al. In vivo amphetamine action is contingent on α CaMKII. Neuropsychopharmacology 39, 2681–2693 (2014).
pubmed: 24871545
pmcid: 4207348
doi: 10.1038/npp.2014.124
Centonze, D. et al. Distinct roles of D1 and D5 dopamine receptors in motor activity and striatal synaptic plasticity. J. Neurosci. 23, 8506–8512 (2003).
pubmed: 13679419
pmcid: 6740372
doi: 10.1523/JNEUROSCI.23-24-08506.2003
Dourado, M., Cardoso-Cruz, H., Monteiro, C. & Galhardo, V. Effect of motor impairment on analgesic efficacy of dopamine D2/3 receptors in a rat model of neuropathy. J. Exp. Neurosci. 10, JEN.S36492 (2016).
doi: 10.4137/JEN.S36492
Radl, D. et al. Differential regulation of striatal motor behavior and related cellular responses by dopamine D2L and D2S isoforms. Proc. Natl Acad. Sci. USA 115, 198–203 (2018).
pubmed: 29255027
doi: 10.1073/pnas.1717194115
Paxinos, G. & Franklin, K. B. Paxinos and Franklin’s the Mouse Brain in Stereotaxic Coordinates, Compact, 5th Edition (Academic Press, 2019).
Cliburn, R. A. et al. Immunochemical localization of vesicular monoamine transporter 2 (VMAT2) in mouse brain. J. Chem. Neuroanat. 83–84, 82–90 (2017).
pubmed: 27836486
doi: 10.1016/j.jchemneu.2016.11.003
Isingrini, E. et al. Genetic elimination of dopamine vesicular stocks in the nigrostriatal pathway replicates Parkinson’s disease motor symptoms without neuronal degeneration in adult mice. Sci. Rep. 7, 12432 (2017).