Cell-type-specific asynchronous modulation of PKA by dopamine in learning

Nature



  • 1.

    Bromberg-Martin, E. S., Matsumoto, M. & Hikosaka, O. Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 68, 815–834 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 2.

    Kravitz, A. V. & Kreitzer, A. C. Striatal mechanisms underlying movement, reinforcement, and punishment. Physiology (Bethesda) 27, 167–177 (2012).


    Google Scholar
     




  • 3.

    Vidal-Gadea, A. G. & Pierce-Shimomura, J. T. Conserved role of dopamine in the modulation of behavior. Commun. Integr. Biol. 5, 440–447 (2012).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 4.

    Steinberg, E. E. et al. Positive reinforcement mediated by midbrain dopamine neurons requires D1 and D2 receptor activation in the nucleus accumbens. PLoS ONE 9, e94771 (2014).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     




  • 5.

    Hikida, T., Kimura, K., Wada, N., Funabiki, K. & Nakanishi, S. Distinct roles of synaptic transmission in direct and indirect striatal pathways to reward and aversive behavior. Neuron 66, 896–907 (2010).

    CAS 
    PubMed 
    Article 

    Google Scholar
     




  • 6.

    Tsai, H. C. et al. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324, 1080–1084 (2009).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 7.

    Steinberg, E. E. et al. A causal link between prediction errors, dopamine neurons and learning. Nat. Neurosci. 16, 966–973 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 8.

    Saunders, B. T., Richard, J. M., Margolis, E. B. & Janak, P. H. Dopamine neurons create Pavlovian conditioned stimuli with circuit-defined motivational properties. Nat. Neurosci. 21, 1072–1083 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 9.

    Coddington, L. T. & Dudman, J. T. The timing of action determines reward prediction signals in identified midbrain dopamine neurons. Nat. Neurosci. 21, 1563–1573 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 10.

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

    CAS 
    PubMed 
    Article 

    Google Scholar
     




  • 11.

    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).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 12.

    Eshel, N., Tian, J., Bukwich, M. & Uchida, N. Dopamine neurons share common response function for reward prediction error. Nat. Neurosci. 19, 479–486 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 13.

    Day, J. J., Roitman, M. F., Wightman, R. M. & Carelli, R. M. Associative learning mediates dynamic shifts in dopamine signaling in the nucleus accumbens. Nat. Neurosci. 10, 1020–1028 (2007).

    CAS 
    PubMed 
    Article 

    Google Scholar
     




  • 14.

    Shen, W., Flajolet, M., Greengard, P. & Surmeier, D. J. Dichotomous dopaminergic control of striatal synaptic plasticity. Science 321, 848–851 (2008).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 15.

    Gerfen, C. R. et al. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250, 1429–1432 (1990).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar
     




  • 16.

    Kupchik, Y. M. et al. Coding the direct/indirect pathways by D1 and D2 receptors is not valid for accumbens projections. Nat. Neurosci. 18, 1230–1232 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 17.

    Skeberdis, V. A. et al. Protein kinase A regulates calcium permeability of NMDA receptors. Nat. Neurosci. 9, 501–510 (2006).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     




  • 18.

    Lee, H. K. et al. Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112, 631–643 (2003).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     




  • 19.

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

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 20.

    Iino, Y. et al. Dopamine D2 receptors in discrimination learning and spine enlargement. Nature 579, 555–560 (2020).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar
     




  • 21.

    Lau, G. C., Saha, S., Faris, R. & Russek, S. J. Up-regulation of NMDAR1 subunit gene expression in cortical neurons via a PKA-dependent pathway. J. Neurochem. 88, 564–575 (2004).

    CAS 
    PubMed 
    Article 

    Google Scholar
     




  • 22.

    Nayak, A., Zastrow, D. J., Lickteig, R., Zahniser, N. R. & Browning, M. D. Maintenance of late-phase LTP is accompanied by PKA-dependent increase in AMPA receptor synthesis. Nature 394, 680–683 (1998).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar
     




  • 23.

    Lee, S. J., Chen, Y., Lodder, B. & Sabatini, B. L. Monitoring behaviorally induced biochemical changes using fluorescence lifetime photometry. Front. Neurosci. 13, 766 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 24.

    Chen, Y., Saulnier, J. L., Yellen, G. & Sabatini, B. L. A PKA activity sensor for quantitative analysis of endogenous GPCR signaling via 2-photon FRET-FLIM imaging. Front. Pharmacol. 5, 56 (2014).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     




  • 25.

    Chen, Y. et al. Endogenous Gαq-coupled neuromodulator receptors activate protein kinase A. Neuron 96, 1070–1083.e5 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 26.

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

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 27.

    Dana, H. et al. Sensitive red protein calcium indicators for imaging neural activity. eLife 5, e12727 (2016).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     




  • 28.

    Patriarchi, T. et al. Ultrafast neuronal imaging of dopamine dynamics with designed genetically encoded sensors. Science 360, eaat4422 (2018).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     




  • 29.

    Klapoetke, N. C. et al. Independent optical excitation of distinct neural populations. Nat. Methods 11, 338–346 (2014).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 30.

    Mahn, M. et al. High-efficiency optogenetic silencing with soma-targeted anion-conducting channelrhodopsins. Nat. Commun. 9, 4125 (2018).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     




  • 31.

    Howe, M. W., Tierney, P. L., Sandberg, S. G., Phillips, P. E. M. & Graybiel, A. M. Prolonged dopamine signalling in striatum signals proximity and value of distant rewards. Nature 500, 575–579 (2013).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 32.

    Matamales, M. et al. Local D2- to D1-neuron transmodulation updates goal-directed learning in the striatum. Science 367, 549–555 (2020).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar
     




  • 33.

    Jiang, S. Z. et al. NCS-Rapgef2, the protein product of the neuronal Rapgef2 gene, is a specific activator of D1 dopamine receptor-dependent ERK phosphorylation in mouse brain. eNeuro 4, ENEURO.0248-17.2017 (2017).

    Article 

    Google Scholar
     




  • 34.

    Ilango, A. et al. Similar roles of substantia nigra and ventral tegmental dopamine neurons in reward and aversion. J. Neurosci. 34, 817–822 (2014).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 35.

    Goto, A. et al. Circuit-dependent striatal PKA and ERK signaling underlies rapid behavioral shift in mating reaction of male mice. Proc. Natl Acad. Sci. USA 112, 6718–6723 (2015).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar
     




  • 36.

    Yamaguchi, T. et al. Role of PKA signaling in D2 receptor-expressing neurons in the core of the nucleus accumbens in aversive learning. Proc. Natl Acad. Sci. USA 112, 11383–11388 (2015).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar
     




  • 37.

    Ma, L. et al. A highly sensitive A-kinase activity reporter for imaging neuromodulatory events in awake mice. Neuron 99, 665–679.e5 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 38.

    Collins, A. G. E. & Frank, M. J. Opponent actor learning (OpAL): modeling interactive effects of striatal dopamine on reinforcement learning and choice incentive. Psychol. Rev. 121, 337–366 (2014).

    PubMed 
    Article 

    Google Scholar
     




  • 39.

    Gurney, K. N., Humphries, M. D. & Redgrave, P. A new framework for cortico-striatal plasticity: behavioural theory meets in vitro data at the reinforcement-action interface. PLoS Biol. 13, e1002034 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     




  • 40.

    Gerfen, C. R. & Surmeier, D. J. Modulation of striatal projection systems by dopamine. Annu. Rev. Neurosci. 34, 441–466 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 41.

    Gerfen, C. R., Paletzki, R. & Heintz, N. GENSAT BAC Cre-recombinase driver lines to study the functional organization of cerebral cortical and basal ganglia circuits. Neuron 80, 1368–1383 (2013).

    CAS 
    PubMed 
    Article 

    Google Scholar
     




  • 42.

    Bäckman, 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 
    Article 
    CAS 

    Google Scholar
     




  • 43.

    Lee, S. J., Escobedo-Lozoya, Y., Szatmari, E. M. & Yasuda, R. Activation of CaMKII in single dendritic spines during long-term potentiation. Nature 458, 299–304 (2009).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     




  • 44.

    Pnevmatikakis, E. A. et al. Simultaneous denoising, deconvolution, and demixing of calcium imaging data. Neuron 89, 285–299 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     


  • 45.

    Motulsky, H. J. How to report the methods used for the mixed model analysis https://www.graphpad.com/guides/prism/8/statistics/stat_how-to-report-the-methods-used.htm (2020).

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