Categories: NATURE

Dopamine dynamics are dispensable for movement but promote reward responses


  • Liu, C., Goel, P. & Kaeser, P. S. Spatial and temporal scales of dopamine transmission. Nat. Rev. Neurosci. 22, 345–358 (2021).

    Article 

    Google Scholar
     

  • Grace, A. A. Dysregulation of the dopamine system in the pathophysiology of schizophrenia and depression. Nat. Rev. Neurosci. 17, 524–532 (2016).

    Article 
    CAS 

    Google Scholar
     

  • 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).

    Article 
    ADS 

    Google Scholar
     

  • Howe, M. W. & Dombeck, D. A. Rapid signalling in distinct dopaminergic axons during locomotion and reward. Nature 535, 505–510 (2016).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Dodson, P. D. et al. Representation of spontaneous movement by dopaminergic neurons is cell-type selective and disrupted in parkinsonism. Proc. Natl Acad. Sci. USA 113, E2180–E2188 (2016).

    Article 
    CAS 

    Google Scholar
     

  • Jin, X. & Costa, R. M. Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature 466, 457–462 (2010).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Berke, J. D. What does dopamine mean? Nat. Neurosci. https://doi.org/10.1038/s41593-018-0152-y (2018).

  • Coddington, L. T. & Dudman, J. T. Learning from action: reconsidering movement signaling in midbrain dopamine neuron activity. Neuron 104, 63–77 (2019).

    Article 
    CAS 

    Google Scholar
     

  • Schultz, W. Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 30, 259–288 (2007).

    Article 
    CAS 

    Google Scholar
     

  • Schultz, W., Dayan, P. & Montague, P. R. A neural substrate of prediction and reward. Science 275, 1593–1599 (1997).

    Article 
    CAS 

    Google Scholar
     

  • Kim, H. R. et al. A unified framework for dopamine signals across timescales. Cell 183, 1600–1616.e25 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Amo, R. et al. A gradual temporal shift of dopamine responses mirrors the progression of temporal difference error in machine learning. Nat. Neurosci. 25, 1082–1092 (2022).

    Article 
    CAS 

    Google Scholar
     

  • Watabe-Uchida, M., Eshel, N. & Uchida, N. Neural circuitry of reward prediction error. Annu. Rev. Neurosci. 40, 373–394 (2017).

    Article 
    CAS 

    Google Scholar
     

  • Poewe, W. et al. Parkinson disease. Nat. Rev. Dis. Primers 3, 17013 (2017).

    Article 

    Google Scholar
     

  • Cotzias, G. C., Van Woert, M. H. & Schiffer, L. M. Aromatic amino acids and modification of parkinsonism. N. Engl. J. Med. 276, 374–379 (1967).

    Article 
    CAS 

    Google Scholar
     

  • Carlsson, A. A paradigm shift in brain research. Science 294, 1021–1024 (2001).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Carlsson, A. On the problem of the mechanism of action of some psychopharmaca. Psychiatr. Neurol. 140, 220–222 (1960).

    Article 
    CAS 

    Google Scholar
     

  • Bakhurin, K. et al. Force tuning explains changes in phasic dopamine signaling during stimulus-reward learning. Preprint at bioRxiv https://doi.org/10.1101/2023.04.23.537994 (2023).

  • Jeong, H. et al. Mesolimbic dopamine release conveys causal associations. Science 378, eabq6740 (2022).

    Article 
    CAS 

    Google Scholar
     

  • Berridge, K. C., Robinson, T. E. & Aldridge, J. W. Dissecting components of reward: ‘liking’, ‘wanting’, and learning. Curr. Opin. Pharmacol. 9, 65–73 (2009).

    Article 
    CAS 

    Google Scholar
     

  • Niv, Y., Daw, N. D., Joel, D. & Dayan, P. Tonic dopamine: opportunity costs and the control of response vigor. Psychopharmacology 191, 507–520 (2007).

    Article 
    CAS 

    Google Scholar
     

  • Hamilos, A. E. et al. Slowly evolving dopaminergic activity modulates the moment-to-moment probability of reward-related self-timed movements. eLife 10, e62583 (2021).

    Article 
    CAS 

    Google Scholar
     

  • Mohebi, A. et al. Dissociable dopamine dynamics for learning and motivation. Nature 570, 65–70 (2019).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Howe, M. et al. Coordination of rapid cholinergic and dopaminergic signaling in striatum during spontaneous movement. eLife 8, e44903 (2019).

    Article 

    Google Scholar
     

  • Yagishita, S. et al. A critical time window for dopamine actions on the structural plasticity of dendritic spines. Science 345, 1616–1620 (2014).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Chaudhury, D. et al. Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature 493, 532–536 (2013).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Crego, A. C. G. et al. Complementary control over habits and behavioral vigor by phasic activity in the dorsolateral striatum. J. Neurosci. 40, 2139–2153 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Bova, A. et al. Precisely timed dopamine signals establish distinct kinematic representations of skilled movements. eLife 9, e61591 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Howard, C. D., Li, H., Geddes, C. E. & Jin, X. Dynamic nigrostriatal dopamine biases action selection. Neuron 93, 1436–1450.e8 (2017).

    Article 
    CAS 

    Google Scholar
     

  • Liu, C. et al. An action potential initiation mechanism in distal axons for the control of dopamine release. Science 375, 1378–1385 (2022).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Sun, F. et al. Next-generation GRAB sensors for monitoring dopaminergic activity in vivo. Nat. Methods 17, 1156–1166 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Patriarchi, T. et al. An expanded palette of dopamine sensors for multiplex imaging in vivo. Nat. Methods 17, 1147–1155 (2020).

    Article 
    CAS 

    Google Scholar
     

  • 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).

    Article 
    CAS 

    Google Scholar
     

  • Banerjee, A. et al. Molecular and functional architecture of striatal dopamine release sites. Neuron 110, 248–265.e9 (2022).

    Article 
    CAS 

    Google Scholar
     

  • Robinson, B. G. et al. RIM is essential for stimulated but not spontaneous somatodendritic dopamine release in the midbrain. eLife 8, e47972 (2019).

    Article 
    CAS 

    Google Scholar
     

  • Zych, S. M. & Ford, C. P. Divergent properties and independent regulation of striatal dopamine and GABA co-transmission. Cell Rep. 39, 110823 (2022).

    Article 
    CAS 

    Google Scholar
     

  • Parker, J. G. et al. Absence of NMDA receptors in dopamine neurons attenuates dopamine release but not conditioned approach during Pavlovian conditioning. Proc. Natl Acad. Sci. USA 107, 13491–13496 (2010).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • 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).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Grace, A. A. & Bunney, B. S. The control of firing pattern in nigral dopamine neurons: burst firing. J. Neurosci. 4, 2877–2890 (1984).

    Article 
    CAS 

    Google Scholar
     

  • Grace, A. A. & Bunney, B. S. The control of firing pattern in nigral dopamine neurons: single spike firing. J. Neurosci. 4, 2866–2876 (1984).

    Article 
    CAS 

    Google Scholar
     

  • 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).

    Article 
    CAS 

    Google Scholar
     

  • Ungerstedt, U. Postsynaptic supersensitivity after 6-hydroxy-dopamine induced degeneration of the nigro-striatal dopamine system. Acta Physiol. Scand. Suppl. 367, 69–93 (1971).

    Article 
    CAS 

    Google Scholar
     

  • Keefe, K. A., Salamone, J. D., Zigmond, M. J. & Stricker, E. M. Paradoxical kinesia in parkinsonism is not caused by dopamine release. Studies in an animal model. Arch. Neurol. 46, 1070–1075 (1989).

    Article 
    CAS 

    Google Scholar
     

  • Lebowitz, J. J. et al. Synaptotagmin-1 is a Ca2+ sensor for somatodendritic dopamine release. Cell Rep. 42, 111915 (2023).

    Article 
    CAS 

    Google Scholar
     

  • German, P. W. & Fields, H. L. Rat nucleus accumbens neurons persistently encode locations associated with morphine reward. J. Neurophysiol. 97, 2094–2106 (2007).

    Article 

    Google Scholar
     

  • Tsutsui-Kimura, I. et al. Distinct temporal difference error signals in dopamine axons in three regions of the striatum in a decision-making task. eLife 9, e62390 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Berridge, C. W., Stratford, T. L., Foote, S. L. & Kelley, A. E. Distribution of dopamine β-hydroxylase-like immunoreactive fibers within the shell subregion of the nucleus accumbens. Synapse 27, 230–241 (1997).

    Article 
    CAS 

    Google Scholar
     

  • Schroeter, S. et al. Immunolocalization of the cocaine- and antidepressant-sensitive l-norepinephrine transporter. J. Comp. Neurol. 420, 211–232 (2000).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Antonini, A. et al. Effect of levodopa–carbidopa intestinal gel on dyskinesia in advanced Parkinson’s disease patients. Mov. Disord. 31, 530–537 (2016).

    Article 
    CAS 

    Google Scholar
     

  • Flagel, S. B. et al. A selective role for dopamine in stimulus-reward learning. Nature 469, 53–57 (2011).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Dolan, R. J. & Dayan, P. Goals and habits in the brain. Neuron 80, 312–325 (2013).

    Article 
    CAS 

    Google Scholar
     

  • Wang, J. X. et al. Prefrontal cortex as a meta-reinforcement learning system. Nat. Neurosci. 21, 860–868 (2018).

    Article 
    CAS 

    Google Scholar
     

  • Wang, A. Y., Miura, K. & Uchida, N. The dorsomedial striatum encodes net expected return, critical for energizing performance vigor. Nat. Neurosci. 16, 639–647 (2013).

    Article 
    CAS 

    Google Scholar
     

  • Dudman, J. T. & Krakauer, J. W. The basal ganglia: from motor commands to the control of vigor. Curr. Opin. Neurobiol. 37, 158–166 (2016).

    Article 
    CAS 

    Google Scholar
     

  • Seiler, J. L. et al. Dopamine signaling in the dorsomedial striatum promotes compulsive behavior. Curr. Biol. 32, 1175–1188.e5 (2022).

    Article 
    CAS 

    Google Scholar
     

  • van Elzelingen, W. et al. Striatal dopamine signals are region specific and temporally stable across action-sequence habit formation. Curr. Biol. 32, 1163–1174.e6 (2022).

    Article 

    Google Scholar
     

  • Wyvell, C. L. & Berridge, K. C. Intra-accumbens amphetamine increases the conditioned incentive salience of sucrose reward: enhancement of reward ‘wanting’ without enhanced ‘liking’ or response reinforcement. J. Neurosci. 20, 8122–8130 (2000).

    Article 
    CAS 

    Google Scholar
     

  • Cagniard, B. et al. Dopamine scales performance in the absence of new learning. Neuron 51, 541–547 (2006).

    Article 
    CAS 

    Google Scholar
     

  • Yin, H. H., Zhuang, X. & Balleine, B. W. Instrumental learning in hyperdopaminergic mice. Neurobiol. Learn. Mem. 85, 283–288 (2006).

    Article 
    CAS 

    Google Scholar
     

  • Jain, S. et al. Adaptor protein-3 produces synaptic vesicles that release phasic dopamine. Proc. Natl Acad. Sci. USA 120, e2309843120 (2023).

    Article 
    CAS 

    Google Scholar
     

  • Kaeser, P. S. et al. RIM1α and RIM1β are synthesized from distinct promoters of the RIM1 gene to mediate differential but overlapping synaptic functions. J. Neurosci. 28, 13435–13447 (2008).

    Article 
    CAS 

    Google Scholar
     

  • Kaeser, P. S. et al. RIM proteins tether Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 144, 282–295 (2011).

    Article 
    CAS 

    Google Scholar
     

  • Zhou, Q. et al. Architecture of the synaptotagmin–SNARE machinery for neuronal exocytosis. Nature 525, 62–67 (2015).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • 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).

    Article 
    CAS 

    Google Scholar
     

  • Allen Mouse Brain Atlas [mouse, P56, coronal 2011] (Allen Institute for Brain Science, 2004); https://atlas.brain-map.org.

  • Chen, T.-W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295–300 (2013).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Rudolph, S. et al. Cerebellum-specific deletion of the GABAA receptor δ subunit leads to sex-specific disruption of behavior. Cell Rep. 33, 108338 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Newell, A., Yang, K. & Deng, J. Stacked hourglass networks for human pose estimation. In Computer Vision—ECCV 2016. Lecture Notes in Computer Science vol. 9912 (eds Leibe, B., Matas, J., Sebe, N. & Welling, M.) 484–499 (Springer, 2016).

  • Mathis, A. et al. DeepLabCut: markerless pose estimation of user-defined body parts with deep learning. Nat. Neurosci. 21, 1281–1289 (2018).

    Article 
    CAS 

    Google Scholar
     

  • Nath, T. et al. Using DeepLabCut for 3D markerless pose estimation across species and behaviors. Nat. Protoc. 14, 2152–2176 (2019).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Hutchison, M. A. et al. Genetic inhibition of neurotransmission reveals role of glutamatergic input to dopamine neurons in high-effort behavior. Mol. Psychiatry 23, 1213–1225 (2018).

    Article 
    CAS 

    Google Scholar
     

  • Uchida, N. & Mainen, Z. F. Speed and accuracy of olfactory discrimination in the rat. Nat. Neurosci. 6, 1224–1229 (2003).

    Article 
    CAS 

    Google Scholar
     

  • Menegas, W. et al. Dopamine neurons projecting to the posterior striatum form an anatomically distinct subclass. eLife 4, e10032 (2015).

    Article 

    Google Scholar
     

  • Nguyen, N. D. et al. Cortical reactivations predict future sensory responses. Nature 625, 110–118 (2024).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Cai, X. & Kaeser, P. Data table for Cai et al., 2024. Zenodo https://doi.org/10.5281/zenodo.13329864 (2024).

  • Brimblecombe, K. R., Gracie, C. J., Platt, N. J. & Cragg, S. J. 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 (2015).

    Article 
    CAS 

    Google Scholar
     

  • Tedford, H. W. & Zamponi, G. W. Direct G protein modulation of Cav2 calcium channels. Pharmacol. Rev. 58, 837–862 (2006).

    Article 
    CAS 

    Google Scholar
     

  • Pereira, D. B. et al. Fluorescent false neurotransmitter reveals functionally silent dopamine vesicle clusters in the striatum. Nat. Neurosci. 19, 578–586 (2016).

    Article 
    CAS 

    Google Scholar
     

  • Delignat-Lavaud, B. et al. Synaptotagmin-1-dependent phasic axonal dopamine release is dispensable for basic motor behaviors in mice. Nat. Commun. 14, 4120 (2023).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Kaeser, P. S. & Regehr, W. G. Molecular mechanisms for synchronous, asynchronous, and spontaneous neurotransmitter release. Annu. Rev. Physiol. 76, 333–363 (2014).

    Article 
    CAS 

    Google Scholar
     



  • Source link

    fromermedia@gmail.com

    Share
    Published by
    fromermedia@gmail.com

    Recent Posts

    How Digital Marketing is Revolutionizing the Healthcare Industry

    In today’s fast-paced digital era, healthcare organizations are no exception to the power of digital…

    6 hours ago

    Author Correction: Microglia-mediated T cell infiltration drives neurodegeneration in tauopathy

    Department of Neurology, Hope Center for Neurological Disorders, Knight Alzheimer’s Disease Research Center, Washington University…

    8 hours ago

    Star-eating black hole could power cosmic particle accelerator

    Download the Nature Podcast 16 October 2024In this episode:00:46 An unusual γ-ray producing microquasarA type…

    8 hours ago

    Global conservation priorities for island plant diversity

    Schrader, J. et al. Nature https://doi.org/10.1038/s41586-024-08036-1 (2024).Article  Google Scholar  Losos, J. B. & Ricklefs, R.…

    8 hours ago

    High CO2 dampens then amplifies N-induced diversity loss over 24 years

    Stevens, C. J., Dise, N. B., Mountford, J. O. & Gowing, D. J. Impact of…

    8 hours ago

    Most of Earth’s meteorites come from three young asteroid families

    Nature, Published online: 16 October 2024; doi:10.1038/d41586-024-03051-8Researchers have narrowed down the sources of the most…

    8 hours ago