Intrinsic dopamine and acetylcholine dynamics in the striatum of mice.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
Sep 2023
Sep 2023
Historique:
received:
08
06
2022
accepted:
22
03
2023
medline:
22
9
2023
pubmed:
10
8
2023
entrez:
9
8
2023
Statut:
ppublish
Résumé
External rewards such as food and money are potent modifiers of behaviour
Identifiants
pubmed: 37558873
doi: 10.1038/s41586-023-05995-9
pii: 10.1038/s41586-023-05995-9
doi:
Substances chimiques
Acetylcholine
N9YNS0M02X
Dopamine
VTD58H1Z2X
Glutamine
0RH81L854J
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
543-549Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Schultz, W. Behavioral theories and the neurophysiology of reward. Annu. Rev. Psychol. 57, 87–115 (2006).
pubmed: 16318590
doi: 10.1146/annurev.psych.56.091103.070229
O’Doherty, J. P., Cockburn, J. & Pauli, W. M. Learning, reward, and decision making. Annu. Rev. Psychol. 68, 73–100 (2017).
pubmed: 27687119
doi: 10.1146/annurev-psych-010416-044216
Mirenowicz, J. & Schultz, W. Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature 379, 449–451 (1996).
pubmed: 8559249
doi: 10.1038/379449a0
Cohen, J. Y., Haesler, S., Vong, L., Lowell, B. B. & Uchida, N. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482, 85–88 (2012).
pubmed: 22258508
pmcid: 3271183
doi: 10.1038/nature10754
Morris, G., Arkadir, D., Nevet, A., Vaadia, E. & Bergman, H. Coincident but distinct messages of midbrain dopamine and striatal tonically active neurons. Neuron 43, 133–143 (2004).
pubmed: 15233923
doi: 10.1016/j.neuron.2004.06.012
Aosaki, T., Graybiel, A. M. & Kimura, M. Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys. Science 265, 412–415 (1994).
pubmed: 8023166
doi: 10.1126/science.8023166
Costa, R. M. A selectionist account of de novo action learning. Curr. Opin. Neurobiol. 21, 579–586 (2011).
pubmed: 21641793
doi: 10.1016/j.conb.2011.05.004
Coddington, L. T. & Dudman, J. T. Learning from action: reconsidering movement signaling in midbrain dopamine neuron activity. Neuron 104, 63–77 (2019).
pubmed: 31600516
doi: 10.1016/j.neuron.2019.08.036
Berke, J. D. What does dopamine mean? Nat. Neurosci. 21, 787–793 (2018).
pubmed: 29760524
pmcid: 6358212
doi: 10.1038/s41593-018-0152-y
Klaus, A., Alves da Silva, J. & Costa, R. M. What, if, and when to move: basal ganglia circuits and self-paced action initiation. Annu. Rev. Neurosci. 42, 459–483 (2019).
pubmed: 31018098
doi: 10.1146/annurev-neuro-072116-031033
Cox, J. & Witten, I. B. Striatal circuits for reward learning and decision-making. Nat. Rev. Neurosci. 20, 482–494 (2019).
pubmed: 31171839
pmcid: 7231228
doi: 10.1038/s41583-019-0189-2
Shen, W. et al. M4 muscarinic receptor signaling ameliorates striatal plasticity deficits in models of L-DOPA-induced dyskinesia. Neuron 88, 762–773 (2015).
pubmed: 26590347
pmcid: 4864040
doi: 10.1016/j.neuron.2015.10.039
Reynolds, J. N. J. et al. Coincidence of cholinergic pauses, dopaminergic activation and depolarisation of spiny projection neurons drives synaptic plasticity in the striatum. Nat. Commun. 13, 1296 (2022).
pubmed: 35277506
pmcid: 8917208
doi: 10.1038/s41467-022-28950-0
Howe, M. W. & Dombeck, D. A. Rapid signalling in distinct dopaminergic axons during locomotion and reward. Nature 535, 505–510 (2016).
pubmed: 27398617
pmcid: 4970879
doi: 10.1038/nature18942
da Silva, J. A., Tecuapetla, F., Paixao, V. & Costa, R. M. Dopamine neuron activity before action initiation gates and invigorates future movements. Nature 554, 244–248 (2018).
pubmed: 29420469
doi: 10.1038/nature25457
Panigrahi, B. et al. Dopamine is required for the neural representation and control of movement vigor. Cell 162, 1418–1430 (2015).
pubmed: 26359992
doi: 10.1016/j.cell.2015.08.014
Engelhard, B. et al. Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons. Nature 570, 509–513 (2019).
pubmed: 31142844
pmcid: 7147811
doi: 10.1038/s41586-019-1261-9
Mohebi, A. et al. Dissociable dopamine dynamics for learning and motivation. Nature 570, 65–70 (2019).
pubmed: 31118513
pmcid: 6555489
doi: 10.1038/s41586-019-1235-y
Howe, M. et al. Coordination of rapid cholinergic and dopaminergic signaling in striatum during spontaneous movement. eLife 8, e44903 (2019).
pubmed: 30920369
pmcid: 6457892
doi: 10.7554/eLife.44903
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
Threlfell, S. et al. Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 75, 58–64 (2012).
pubmed: 22794260
doi: 10.1016/j.neuron.2012.04.038
Cachope, R. et al. Selective activation of cholinergic interneurons enhances accumbal phasic dopamine release: setting the tone for reward processing. Cell Rep. 2, 33–41 (2012).
pubmed: 22840394
pmcid: 3408582
doi: 10.1016/j.celrep.2012.05.011
Liu, C. et al. An action potential initiation mechanism in distal axons for the control of dopamine release. Science 375, 1378–1385 (2022).
pubmed: 35324301
pmcid: 9081985
doi: 10.1126/science.abn0532
Straub, C., Tritsch, N. X., Hagan, N. A., Gu, C. & Sabatini, B. L. Multiphasic modulation of cholinergic interneurons by nigrostriatal afferents. J. Neurosci. 34, 8557–8569 (2014).
pubmed: 24948810
pmcid: 4061393
doi: 10.1523/JNEUROSCI.0589-14.2014
Chuhma, N., Mingote, S., Moore, H. & Rayport, S. Dopamine neurons control striatal cholinergic neurons via regionally heterogeneous dopamine and glutamate signaling. Neuron 81, 901–912 (2014).
pubmed: 24559678
pmcid: 3933825
doi: 10.1016/j.neuron.2013.12.027
Sun, F. et al. Next-generation GRAB sensors for monitoring dopaminergic activity in vivo. Nat. Methods 17, 1156–1166 (2020).
pubmed: 33087905
pmcid: 7648260
doi: 10.1038/s41592-020-00981-9
Jing, M. et al. An optimized acetylcholine sensor for monitoring in vivo cholinergic activity. Nat. Methods 17, 1139–1146 (2020).
pubmed: 32989318
pmcid: 7606762
doi: 10.1038/s41592-020-0953-2
Tritsch, N. X. & Sabatini, B. L. Dopaminergic modulation of synaptic transmission in cortex and striatum. Neuron 76, 33–50 (2012).
pubmed: 23040805
pmcid: 4386589
doi: 10.1016/j.neuron.2012.09.023
Hnasko, T. S. et al. Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo. Neuron 65, 643–656 (2010).
pubmed: 20223200
pmcid: 2846457
doi: 10.1016/j.neuron.2010.02.012
Tritsch, N. X., Ding, J. B. & Sabatini, B. L. Dopaminergic neurons inhibit striatal output through non-canonical release of GABA. Nature 490, 262–266 (2012).
pubmed: 23034651
pmcid: 3944587
doi: 10.1038/nature11466
Shin, J. H., Adrover, M. F., Wess, J. & Alvarez, V. A. Muscarinic regulation of dopamine and glutamate transmission in the nucleus accumbens. Proc. Natl Acad. Sci. USA 112, 8124–8129 (2015).
pubmed: 26080439
pmcid: 4491757
doi: 10.1073/pnas.1508846112
Joshua, M. et al. Synchronization of midbrain dopaminergic neurons is enhanced by rewarding events. Neuron 62, 695–704 (2009).
pubmed: 19524528
doi: 10.1016/j.neuron.2009.04.026
Liu, C., Goel, P. & Kaeser, P. S. Spatial and temporal scales of dopamine transmission. Nat. Rev. Neurosci. 22, 345–358 (2021).
pubmed: 33837376
pmcid: 8220193
doi: 10.1038/s41583-021-00455-7
Fujisawa, S. & Buzsaki, G. A 4 Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities. Neuron 72, 153–165 (2011).
pubmed: 21982376
pmcid: 3235795
doi: 10.1016/j.neuron.2011.08.018
Watabe-Uchida, M., Zhu, L., Ogawa, S. K., Vamanrao, A. & Uchida, N. Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron 74, 858–873 (2012).
pubmed: 22681690
doi: 10.1016/j.neuron.2012.03.017
Guo, Q. et al. Whole-brain mapping of inputs to projection neurons and cholinergic interneurons in the dorsal striatum. PLoS ONE 10, e0123381 (2015).
pubmed: 25830919
pmcid: 4382118
doi: 10.1371/journal.pone.0123381
Neske, G. T. Sleepy circuits in vigilant mice? A slow cortical oscillation occurring during multiple arousal states. J. Neurosci. 37, 7294–7296 (2017).
pubmed: 28768793
pmcid: 6596704
doi: 10.1523/JNEUROSCI.1373-17.2017
Nacher, V., Ledberg, A., Deco, G. & Romo, R. Coherent delta-band oscillations between cortical areas correlate with decision making. Proc. Natl Acad. Sci. USA 110, 15085–15090 (2013).
pubmed: 23980180
pmcid: 3773764
doi: 10.1073/pnas.1314681110
Lee, K. et al. Gain modulation by corticostriatal and thalamostriatal input signals during reward-conditioned behavior. Cell Rep. 29, 2438–2449 (2019).
pubmed: 31747611
pmcid: 6907740
doi: 10.1016/j.celrep.2019.10.060
Quick, M. W. & Lester, R. A. Desensitization of neuronal nicotinic receptors. J. Neurobiol. 53, 457–478 (2002).
pubmed: 12436413
doi: 10.1002/neu.10109
Maskos, U. et al. Nicotine reinforcement and cognition restored by targeted expression of nicotinic receptors. Nature 436, 103–107 (2005).
pubmed: 16001069
doi: 10.1038/nature03694
Choi, S. J. et al. Alterations in the intrinsic properties of striatal cholinergic interneurons after dopamine lesion and chronic L-DOPA. eLife 9, e56920 (2020).
pubmed: 32687053
pmcid: 7380940
doi: 10.7554/eLife.56920
Mamaligas, A. A., Barcomb, K. & Ford, C. P. Cholinergic transmission at muscarinic synapses in the striatum is driven equally by cortical and thalamic inputs. Cell Rep. 28, 1003–1014 (2019).
pubmed: 31340139
pmcid: 6830446
doi: 10.1016/j.celrep.2019.06.077
Zhang, Y. F., Reynolds, J. N. J. & Cragg, S. J. Pauses in cholinergic interneuron activity are driven by excitatory input and delayed rectification, with dopamine modulation. Neuron 98, 918–925 (2018).
pubmed: 29754751
pmcid: 5993868
doi: 10.1016/j.neuron.2018.04.027
Beeler, J. A. & Kisbye Dreyer, J. Synchronicity: the role of midbrain dopamine in whole-brain coordination. eNeuro 6, ENEURO.0345-18.2019 (2019).
Shen, W., Flajolet, M., Greengard, P. & Surmeier, D. J. Dichotomous dopaminergic control of striatal synaptic plasticity. Science 321, 848–851 (2008).
pubmed: 18687967
pmcid: 2833421
doi: 10.1126/science.1160575
Liu, Y., Mattar, M. G., Behrens, T. E. J., Daw, N. D. & Dolan, R. J. Experience replay is associated with efficient nonlocal learning. Science 372, eabf1357 (2021).
pubmed: 34016753
pmcid: 7610948
doi: 10.1126/science.abf1357
Graybiel, A. M. The basal ganglia and chunking of action repertoires. Neurobiol. Learn. Mem. 70, 119–136 (1998).
pubmed: 9753592
doi: 10.1006/nlme.1998.3843
Soares, S., Atallah, B. V. & Paton, J. J. Midbrain dopamine neurons control judgment of time. Science 354, 1273–1277 (2016).
pubmed: 27940870
doi: 10.1126/science.aah5234
Liu, Y., Nour, M. M., Schuck, N. W., Behrens, T. E. J. & Dolan, R. J. Decoding cognition from spontaneous neural activity. Nat. Rev. Neurosci. 23, 204–214 (2022).
pubmed: 35260845
doi: 10.1038/s41583-022-00570-z
Patel, J. C., Rossignol, E., Rice, M. E. & Machold, R. P. Opposing regulation of dopaminergic activity and exploratory motor behavior by forebrain and brainstem cholinergic circuits. Nat. Commun. 3, 1172 (2012).
pubmed: 23132022
doi: 10.1038/ncomms2144
Burbridge, T. J. et al. Visual circuit development requires patterned activity mediated by retinal acetylcholine receptors. Neuron 84, 1049–1064 (2014).
pubmed: 25466916
pmcid: 4258148
doi: 10.1016/j.neuron.2014.10.051
Backman, C. M. et al. Characterization of a mouse strain expressing Cre recombinase from the 3′ untranslated region of the dopamine transporter locus. Genesis 44, 383–390 (2006).
pubmed: 16865686
doi: 10.1002/dvg.20228
Chen, T. W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295–300 (2013).
pubmed: 23868258
pmcid: 3777791
doi: 10.1038/nature12354
Thiele, S. L., Warre, R. & Nash, J. E. Development of a unilaterally-lesioned 6-OHDA mouse model of Parkinson’s disease. J. Vis. Exp. https://doi.org/10.3791/3234 (2012).
Yang, C. F. et al. Sexually dimorphic neurons in the ventromedial hypothalamus govern mating in both sexes and aggression in males. Cell 153, 896–909 (2013).
pubmed: 23663785
pmcid: 3767768
doi: 10.1016/j.cell.2013.04.017
Warren, R. A. et al. A rapid whisker-based decision underlying skilled locomotion in mice. eLife 10, e63596 (2021).
pubmed: 33428566
pmcid: 7800376
doi: 10.7554/eLife.63596
Yang, L., Lee, K., Villagracia, J. & Masmanidis, S. C. Open source silicon microprobes for high throughput neural recording. J. Neural Eng. 17, 016036 (2020).
pubmed: 31731284
pmcid: 7227378
doi: 10.1088/1741-2552/ab581a
Stanford Research Systems. About lock-in amplifiers. https://www.thinksrs.com/downloads/pdfs/applicationnotes/AboutLIAs.pdf (2016).
Balakrishnan, H. & Verghese, G. Modulation and demodulation. http://web.mit.edu/6.02/www/s2012/handouts/14.pdf (2012).
Zutshi, I., Valero, M., Fernandez-Ruiz, A. & Buzsaki, G. Extrinsic control and intrinsic computation in the hippocampal CA1 circuit. Neuron 110, 658–673 (2022).
pubmed: 34890566
doi: 10.1016/j.neuron.2021.11.015
Berke, J. D., Okatan, M., Skurski, J. & Eichenbaum, H. B. Oscillatory entrainment of striatal neurons in freely moving rats. Neuron 43, 883–896 (2004).
pubmed: 15363398
doi: 10.1016/j.neuron.2004.08.035
Schmitzer-Torbert, N. C. & Redish, A. D. Task-dependent encoding of space and events by striatal neurons is dependent on neural subtype. Neuroscience 153, 349–360 (2008).
pubmed: 18406064
doi: 10.1016/j.neuroscience.2008.01.081
Sharott, A., Doig, N. M., Mallet, N. & Magill, P. J. Relationships between the firing of identified striatal interneurons and spontaneous and driven cortical activities in vivo. J. Neurosci. 32, 13221–13236 (2012).
pubmed: 22993438
pmcid: 4242971
doi: 10.1523/JNEUROSCI.2440-12.2012
Yamin, H. G., Stern, E. A. & Cohen, D. Parallel processing of environmental recognition and locomotion in the mouse striatum. J. Neurosci. 33, 473–484 (2013).
pubmed: 23303928
pmcid: 6704900
doi: 10.1523/JNEUROSCI.4474-12.2013
Peters, A. J., Fabre, J. M. J., Steinmetz, N. A., Harris, K. D. & Carandini, M. Striatal activity topographically reflects cortical activity. Nature 591, 420–425 (2021).
pubmed: 33473213
pmcid: 7612253
doi: 10.1038/s41586-020-03166-8
Gage, G. J., Stoetzner, C. R., Wiltschko, A. B. & Berke, J. D. Selective activation of striatal fast-spiking interneurons during choice execution. Neuron 67, 466–479 (2010).
pubmed: 20696383
pmcid: 2920892
doi: 10.1016/j.neuron.2010.06.034