The role of the striatum in motor learning is addressed. Modern molecular genetic approaches have made it possible to take a closer look at the involvement of neurons of the direct and indirect pathways in various aspects of motor learning. Animal studies have provided evidence that with the critical involvement of the dopaminergic system, direct pathway neurons play a key role in forming and maintaining movements frequently performed in a given context, to the level of taking part in the mechanisms automating these movements, while indirect pathway neurons play a key role in the flexible involvement of particular movements in specific situations. These effects of the activity of the two pathways are probably mediated via their complementary influences on the mechanisms supporting behavioral variability.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alcacer, C., Andreoli, L., Sebastianutto, I., et al., “Chemogenetic stimulation of striatal projection neurons modulates responses to Parkinson’s disease therapy,” J. Clin. Invest., 127, No. 2, 720–734 (2017), https://doi.org/10.1172/JCI90132.
Anderson, M. E. and Horak, F. B., “Influence of the globus pallidus on arm movements in monkeys. III. Timing of movement-related information,” J. Neurophysiol., 54, No. 2, 433–48 (1985), https://doi.org/10.1152/jn.1985.54.2.433.
Ashby, F. G., Ennis, J. M., and Spiering, B. J., “A neurobiological theory of automaticity in perceptual categorization,” Psychol. Rev., 114, No. 3, 632–56 (2007), https://doi.org/10.1037/0033-295X.114.3.632.
Atallah, H. E., Lopez-Paniagua, D., Rudy, J. W., and O’Reilly, R. C., “Separate neural substrates for skill learning and performance in the ventral and dorsal striatum,” Nat. Neurosci., 10, No. 1, 126–31 (2007), https://doi.org/10.1038/nn1817.
Bakhurin, K. I., Li, X., Friedman, A. D., et al., “Opponent regulation of action performance and timing by striatonigral and striatopallidal pathways,” eLife, 9, e54831 (2020), https://doi.org/10.7554/eLife.54831.
Balleine, B. W., “The meaning of behavior: discriminating reflex and volition in the brain,” Neuron, 104, No. 1, 47–62 (2019), https://doi.org/10.1016/j.neuron.2019.09.024.
Bariselli, S., Fobbs, W. C., Creed, M. C., and Kravitz, A. V., “A competitive model for striatal action selection,” Brain Res., 1713, 70–79 (2019), https://doi.org/10.1016/j.brainres.2018.10.009.
Bernstein, N. A., The Construction of Movements, Nauka, Moscow (1947).
Bova, A., Gaidica, M., Hurst, A., et al., “Precisely timed dopamine signals establish distinct kinematic representations of skilled movements,” eLife, 9, e61591 (2020), https://doi.org/10.7554/eLife.61591.
Burnette, E. M., Grodin, E. N., Schacht, J. P., and Ray, L. A., “Clinical and neural correlates of reward and relief drinking,” Alcohol Clin. Exp. Res., 45, No. 1, 194–203 (2021), https://doi.org/10.1111/acer.14495.
Cacciapaglia, F., Wightman, R. M., and Carelli, R. M., “Rapid dopamine signaling differentially modulates distinct microcircuits within the nucleus accumbens during sucrose-directed behavior,” J. Neurosci., 31, No. 39, 13860–13869 (2011), https://doi.org/10.1523/JNEUROSCI.1340-11.2011.
Calabresi, P. and Di Filippo, M., “Neuroscience: Brain’s traffic lights,” Nature, 466, No. 7305, 449 (2010), https://doi.org/10.1038/466449a.
Caveney, S., Cladman, W., Verellen, L., and Donly, C., “Ancestry of neuronal monoamine transporters in the Metazoa,” J. Exp. Biol., 209, 4858–4868 (2006), https://doi.org/10.1242/jeb.02607.
Ceceli, A. O., Natsheh, J. Y., Cruz, D., and Tricomi, E., “The neurobehavioral mechanisms of motivational control in attention-defi cit/hyperactivity disorder,” Cortex, 127, 191–207 (2020), https://doi.org/10.1016/j.cortex.2020.02.009.
Chang, C. Y., Esber, G. R., Marrero-Garcia, Y., et al., “Brief optogenetic inhibition of dopamine neurons mimics endogenous negative reward prediction errors,” Nat. Neurosci., 19, No. 1, 111 (2016), https://doi.org/10.1038/nn.4191.
Choi, Y., Shin, E. Y., and Kim, S., “Spatiotemporal dissociation of fMRI activity in the caudate nucleus underlies human de novo motor skill learning,” Proc. Natl. Acad. Sci. USA, 117, No. 38, 23886–23897 (2020), https://doi.org/10.1073/pnas.2003963117.
Coddington, L. T. and Dudman, J. T., “Learning from action: reconsidering movement signaling in midbrain dopamine neuron activity,” Neuron, 104, No. 1, 63–77 (2019), https://doi.org/10.1016/j.neuron.2019.08.036.
Coddington, L. T. and Dudman, J. T., “The timing of action determines reward prediction signals in identified midbrain dopamine neurons,” Nat. Neurosci., 21, No. 11, 1563–1573 (2018), https://doi.org/10.1038/s41593-018-0245-7.
Cover, K. K., Gyawali, U., Kerkhoff, W. G., at al., “Activation of the Rostral Intralaminar Thalamus Drives Reinforcement through Stria tal Dopamine Release,” Cell Rep., 26, No. 6, 1389–1398.e3 (2019), https://doi.org/10.1016/j.celrep.2019.01.044.
Crego, A. C. G., Štoček, F., Marchuk, A. G., at al., “Complementary control over habits and behavioral vigor by phasic activity in the dorsolateral striatum,” J. Neurosci., 40, No. 10, 2139–2153 (2020), https://doi.org/10.1523/JNEUROSCI.1313-19.2019.
Cui, G., Jun, S. B., Jin, X., at al., “Concurrent activation of striatal direct and indirect pathways during action initiation,” Nature, 494, No. 7436, 238–242 (2013), https://doi.org/10.1038/nature11846.
da Silva, J. A., Tecuapetla, F., Paixão, V., and Costa, R. M., “Dopamine neuron activity before action initiation gates and invigorates future movements,” Nature, 554, No. 7691, 244–248 (2018), https://doi.org/10.1038/nature25457.
Damodaran, S., Evans, R. C., and Blackwell, K. T., “Synchronized firing of fast-spiking interneurons is critical to maintain balanced fi ring between direct and indirect pathway neurons of the striatum,” J. Neurophysiol., 111, No. 4, 836–48 (2014), https://doi.org/10.1152/jn.00382.2013.
Daw, N. D., “Are we of two minds?” Nat. Neurosci., 21, No. 11, 1497–1499 (2018), https://doi.org/10.1038/s41593-018-0258-2.
Desmurget, M. and Turner, R. S., “Motor sequences and the basal ganglia: kinematics, not habits,” J. Neurosci., 30, No. 22, 7685–90 (2010), https://doi.org/10.1523/JNEUROSCI.0163-10.2010.
Dhawale, A. K., Miyamoto, Y. R., Smith, M. A., and Ölveczky, B. P., “Adaptive regulation of motor variability,” Curr. Biol., 29, No. 21, 3551–3562, 7 (2019), https://doi.org/10.1016/j.cub.2019.08.052.
Diao, Z., Yao, L., Cheng, Q., et al., “Involvement of midbrain dopamine neuron activity in negative reinforcement learning in mice,” Mol. Neurobiol., 58, No. 11, 5667–5681 (2021), https://doi.org/10.1007/s12035-021-02515-6.
Dickinson, A., “Actions and habits: the development of behavioural autonomy,” Phil. Trans. Roy. Soc. Lond. Ser. B Biol. Sci., 308, No. 1135, 67–78 (1985).
Dodson, P. D., Dreyer, J. K., Jennings, K. A., et al., “Representation of spontaneous movement by dopaminergic neurons is cell-type selective and disrupted in parkinsonism,” Proc. Natl. Acad. Sci. USA, 113, No. 15, E2180–E2188 (2016), https://doi.org/10.1073/pnas.1515941113.
Dudman, J. T. and Krakauer, J. W., “The basal ganglia: from motor commands to the control of vigor,” Curr. Opin. Neurobiol., 37, 158–166 (2016), https://doi.org/10.1016/j.conb.2016.02.005.
Durieux, P. F., Schiffmann, S. N., and de Kerchove d’Exaerde, A., “Differential regulation of motor control and response to dopaminergic drugs by D1R and D2R neurons in distinct dorsal striatum subregions,” EMBO J., 31, No. 3, 640–653 (2012), https://doi.org/10.1038/emboj.2011.400.
Edlow, B. L., Haynes, R. L., Takahashi, E., et al., “Disconnection of the ascending arousal system in traumatic coma,” J. Neuropathol. Exp. Neurol., 72, No. 6, 505–23 (2013), https://doi.org/10.1097/NEN.0b013e3182945bf6.
Engelhard, B., Finkelstein, J., Cox, J., et al., “Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons,” Nature, 570, No. 7762, 509–513 (2019), https://doi.org/10.1038/s41586-019-1261-9.
Eshel, N., Tian, J., Bukwich, M., and Uchida, N., “Dopamine neurons share common response function for reward prediction error,” Nat. Neurosci., 19, No. 3, 479–86 (2016), https://doi.org/10.1038/nn.4239.
Evans, R. C., Twedell, E. L., Zhu, M., et al., “Functional dissection of basal ganglia inhibitory inputs onto substantia nigra dopaminergic neurons,” Cell Rep., 32, No. 11, 108156 (2020), https://doi.org/10.1016/j.celrep.2020.108156.
Flagel, S. B., Clark, J. J., Robinson, T. E., et al., “A selective role for dopamine in stimulus-reward learning,” Nature, 469, No. 7328, 53–7 (2011), https://doi.org/10.1038/nature09588.
Galaj, E. and Ranaldi, R., “Neurobiology of reward-related learning,” Neurosci. Biobehav. Rev., 124, 224–234 (2021), https://doi.org/10.1016/j.neubiorev.2021.02.007.
Garr, E. and Delamater, A. R., “Chemogenetic inhibition in the dorsal striatum reveals regional specifi city of direct and indirect pathway control of action sequencing,” Neurobiol. Learn. Mem., 169, 107169 (2020), https://doi.org/10.1016/j.nlm.2020.107169.
Garr, E. and Delamater, A. R., “Exploring the relationship between actions, habits, and automaticity in an action sequence task,” Learn. Mem., 26, No. 4, 128–132 (2019), https://doi.org/10.1101/lm.048645.118.
Geddes, C. E., Li, H., and Jin, X., “Optogenetic editing reveals the hierarchical organization of learned action sequences,” Cell, 174, No. 1, 32–43.e15 (2018), https://doi.org/10.1016/j.cell.2018.06.012.
Gerfen, C. R. and Surmeier, D. J., “Modulation of striatal projection systems by dopamine,” Annu. Rev. Neurosci., 34, 441–466 (2011).
Goodman, J. and Packard, M. G., “There is more than one kind of extinction learning,” Front. Syst. Neurosci., 13, 16 (2019), https://doi.org/10.3389/fnsys.2019.00016.
Graybiel, A. M. and Grafton, S. T., “The striatum: where skills and habits meet,” Cold Spring Harb. Perspect. Biol., 7, No. 8, a021691 (2015), https://doi.org/10.1101/cshperspect.a021691.
Graybiel, A. M., “Habits, rituals, and the evaluative brain,” Annu. Rev. Neurosci., 31, 359–87 (2008), https://doi.org/10.1146/annurev.neuro.29.051605.112851.
Hamid, A. A., Frank, M. J., and Moore, C. I., “Wave-like dopamine dynamics as a mechanism for spatiotemporal credit assignment,” Cell, 184, No. 10, 2733–2749.e16 (2021), https://doi.org/10.1016/j.cell.2021.03.046.
Hamid, A. A., Pettibone, J. R., Mabrouk, O. S., et al., “Mesolimbic dopamine signals the value of work,” Nat. Neurosci., 19, No. 1, 117–26 (2016), https://doi.org/10.1038/nn.4173.
Hammond, L. J., “The effect of contingency upon the appetitive conditioning of free-operant behavior,” J. Exp. Anal. Behav., 34, No. 3, 297– 304 (1980), https://doi.org/10.1901/jeab.1980.34-297.
Hardwick, R. M., Forrence, A. D., Krakauer, J. W., and Haith, A. M., “Time-dependent competition between goal-directed and habitual response preparation,” Nat. Hum. Behav., 3, No. 12, 1252–1262 (2019), https://doi.org/10.1038/s41562-019-0725-0.
Hartmann, C., Lazar, A., Nessler, B., and Triesch, J., “Where’s the noise? Key features of spontaneous activity and neural variability arise through learning in a deterministic network,” PLoS Comput. Biol., 11, No. 12, e1004640 (2015), https://doi.org/10.1371/journal.pcbi. 1004640.
Hawes, S. L., Evans, R. C., Unruh, B. A., et al., “Multimodal plasticity in dorsal striatum while learning a lateralized navigation task,” J. Neurosci., 35, No. 29, 10535–49 (2015), https://doi.org/10.1523/JNEUROSCI.4415-14.2015.
Hernandez, L. F., Obeso, I., Costa, R. M., et al., “Dopaminergic vulnerability in parkinson disease: The cost of humans’ habitual performance,” Trends Neurosci., 42, No. 6, 375–383 (2019), https://doi.org/10.1016/j.tins.2019.03.007.
Hikosaka, O., Kim, H. F., Amita, H., et al., “Direct and indirect pathways for choosing objects and actions,” Eur. J. Neurosci., 49, No. 5, 637–645 (2019), https://doi.org/10.1111/ejn.13876.
Hikosaka, O., Takikawa, Y., and Kawagoe, R., “Role of the basal ganglia in the control of purposive saccadic eye movements,” Physiol. Rev., 80, 953–978 (2000).
Hikosaka, O., Yasuda, M., Nakamura, K., et al., “Multiple neuronal circuits for variable object-action choices based on short- and longterm memories,” Proc. Natl. Acad. Sci. USA, 116, No. 52, 26313–20 (2019), https://doi.org/10.1073/pnas.1902283116.
Hintiryan, H., Foster, N. N., Bowman, I., et al., “The mouse cortico-striatal projectome,” Nat. Neurosci., 19, No. 8, 1100–1114 (2016), https://doi.org/10.1038/nn.4332.
Hormigo, S., Zhou, J., Chabbert, D., et al., “Basal ganglia output has a permissive non-driving role in a signaled locomotor action mediated by the midbrain,” J. Neurosci., 41, No. 7, 1529–1552 (2021), https://doi.org/10.1523/JNEUROSCI.1067-20.2020.
Howard, C. D., Li, H., Geddes, C. E., and Jin, X., “Dynamic nigrostriatal dopamine biases action selection,” Neuron, 93, No. 6, 1436–1450.e8 (2017), https://doi.org/10.1016/j.neuron.2017.02.029.
Howe, M. W. and Dombeck, D. A., “Rapid signalling in distinct dopaminergic axons during locomotion and reward,” Nature, 535, No. 7613, 505–510 (2016), https://doi.org/10.1038/nature18942.
Howe, M. W., Tierney, P. L., Sandberg, S. G., et al., “Prolonged dopamine signalling in striatum signals proximity and value of distant rewards,” Nature, 500, No. 7464, 575–579 (2013), https://doi.org/10.1038/nature12475.
Hughes, R. N., Bakhurin, K. I., Petter, E. A., et al., “Ventral tegmental dopamine neurons control the impulse vector during motivated behavior,” Curr. Biol., 30, No. 14, 2681–2694.e5 (2020), https://doi.org/10.1016/j.cub.2020.05.003.
Isomura, Y., Takekawa, T., Harukuni, R., et al., “Reward-modulated motor information in identifi ed striatum neurons,” J. Neurosci., 33, No. 25, 10209–20 (2013), https://doi.org/10.1523/JNEUROSCI.0381-13.2013.
Ivliev, D. A. and Ivlieva, N. Yu., “Smooth decreases in neuron activity in the ventral tegmental area of the midbrain in the process of performing a food-procuring movement,” Zh. Vyssh. Nerv. Deyat., 68, No. 3, 265–272 (2018), https://doi.org/10.7868/S0044467718030012.
Ivlieva, N. Y., Timofeeva, N. O., and Ivliev, D. A., “The dopamine impels us to action as suggested by the neuronal activity in the ventral tegmental area during avoidance conditioning,” Russ. J. Cogn. Sci., 1, No. 1–2, 54–64 (2014).
Ivlieva, N. Yu., “The role of the striatum in the organization of voluntary movements,” Zh. Vyssh. Nerv. Deyat., 71, No. 2, 164–183 (2021), https://doi.org/10.31857/S00444677210200522021.
Jenrette, T. A., Logue, J. B., and Horner, K. A., “Lesions of the patch compartment of dorsolateral striatum disrupt stimulus-response learning,” Neuroscience, 415, 161–172 (2019), https://doi.org/10.1016/j.neuroscience.2019.07.033.
Jin, X. and Costa, R. M., “Start/stop signals emerge in nigrostriatal circuits during sequence learning,” Nature, 466, 457–462 (2010), https://doi.org/10.1038/nature09263.
Jin, X., Tecuapetla, F., and Costa, R. M., “Basal ganglia subcircuits distinctively encode the parsing and concatenation of action sequences,” Nat. Neurosci., 17, No. 3, 423–30 (2014), https://doi.org/10.1038/nn.3632.
Kato, S., Fukabori, R., Nishizawa, K., et al., “Action selection and fl exible switching controlled by the intralaminar thalamic neurons,” Cell Rep., 22, No. 9, 2370–2382 (2018), https://doi.org/10.1016/j.celrep.2018.02.016.
Kent, K., Deng, Q., and McNeill, T. H., “Unilateral skill acquisition induces bilateral NMDA receptor subunit composition shifts in the rat sensorimotor striatum,” Brain Res., 1517, 77–86 (2013), https://doi.org/10.1016/j.brainres.2013.04.021.
Kim, H. F. and Hikosaka, O., “Parallel basal ganglia circuits for voluntary and automatic behaviour to reach rewards,” Brain, 138, Pt 7, 1776–800 (2015), https://doi.org/10.1093/brain/awv134.
Kim, H. F., Amita, H., and Hikosaka, O., “Indirect pathway of caudal basal ganglia for rejection of valueless visual objects,” Neuron, 94, No. 4, 920–930.e3 (2017), https://doi.org/10.1016/j.neuron.2017.04.033.
Kim, H. F., Ghazizadeh, A., and Hikosaka, O., “Dopamine neurons encoding long-term memory of object value for habitual behavior,” Cell, 163, No. 5, 1165–1175 (2015), https://doi.org/10.1016/j.cell.2015.10.063.
Kim, H. F., Ghazizadeh, A., and Hikosaka, O., “Separate groups of dopamine neurons innervate caudate head and tail encoding fl exible and stable value memories,” Front. Neuroanat., 8, 120 (2014), https://doi.org/10.3389/fnana.2014.00120.
Klugah-Brown, B., Di, X., Zweerings, J., et al., “Common and separable neural alterations in substance use disorders: A coordinate-based meta-analyses of functional neuroimaging studies in humans,” Hum. Brain Mapp., 41, No. 16, 4459–4477 (2020), https://doi.org/10.1002/hbm.25085.
Knowlton, B. J. and Patterson, T. K., “Habit formation and the striatum,” Curr. Top. Behav. Neurosci., 37, 275–295 (2018), https://doi.org/10.1007/7854_2016_451.
Krakauer, J. W., Ghilardi, M. F., and Ghez, C., “Independent learning of internal models for kinematic and dynamic control of reaching,” Nat. Neurosci., 2, No. 11, 1026–31 (1999), https://doi.org/10.1038/14826.
Krakauer, J. W., Hadjiosif, A. M., Xu, J., et al., “Motor learning,” Compr. Physiol., 9, No. 2, 613–663 (2019), https://doi.org/10.1002/cphy.c170043.
Kravitz, A. V., Tye, L. D., and Kreitzer, A. C., “Distinct roles for direct and indirect pathway striatal neurons in reinforcement,” Nat. Neurosci., 15, No. 6, 816–8 (2012), https://doi.org/10.1038/nn.3100.
Kunimatsu, J., Yamamoto, S., Maeda, K., and Hikosaka, O., “Environmentbased object values learned by local network in the striatum tail,” Proc. Natl. Acad. Sci. USA, 118, No. 4, e2013623118 (2021), https://doi.org/10.1073/pnas.2013623118.
Kupferschmidt, D. A., Juczewski, K., Cui, G., et al., “Parallel, but dissociable, processing in discrete corticostriatal inputs encodes skill learning,” Neuron, 96, No. 2, 476–489.e5 (2017), https://doi.org/10.1016/j.neuron.2017.09.040.
Kutlu, M. G., Zachry, J. E., Melugin, P. R., et al., “Dopamine release in the nucleus accumbens core signals perceived saliency,” Curr. Biol., 31, No. 21, 4748–4761.e8 (2021), https://doi.org/10.1016/j.cub.2021.08.052.
Kwak, S. and Jung, M. W., “Distinct roles of striatal direct and indirect pathways in value-based decision making,” eLife, 8, e46050 (2019), https://doi.org/10.7554/eLife.46050.
Laurent, M., De Backer, J. F., Rial, D., et al., “Bidirectional control of reversal in a dual action task by direct and indirect pathway activation in the dorsolateral striatum in mice,” Front. Behav. Neurosci., 11, 256 (2017), https://doi.org/10.3389/fnbeh.2017.00256.
Lee, K., Claar, L. D., Hachisuka, A., et al., “Temporally restricted dopaminergic control of reward-conditioned movements,” Nat. Neurosci., 23, No. 2, 209–216 (2020), https://doi.org/10.1038/s41593-019-0567-0.
Lee, R. S., Mattar, M. G., Parker, N. F., et al., “Reward prediction error does not explain movement selectivity in DMS-projecting dopamine neurons,” eLife, 8, e42992 (2019), https://doi.org/10.7554/eLife.42992.
Lee, S. J., Lodder, B., Chen, Y., et al., “Cell-type-specifi c asynchronous modulation of PKA by dopamine in learning,” Nature, 590, No. 7846, 451–456 (2021), https://doi.org/10.1038/s41586-020-03050-5.
Lemke, S. M., Ramanathan, D. S., Guo, L., et al., “Emergent modular neural control drives coordinated motor actions,” Nat. Neurosci., 22, No. 7, 1122–1131 (2019), https://doi.org/10.1038/s41593-019-0407-2.
Lemos, J. C., Friend, D. M., Kaplan, A. R., et al., “Enhanced GABA transmission drives bradykinesia following loss of dopamine D2 receptor signaling,” Neuron, 90, No. 4, 824–838 (2016), https://doi.org/10.1016/j.neuron.2016.04.040.
Lipton, D. M., Gonzales, B. J., and Citri, A., “Dorsal striatal circuits for habits, compulsions and addictions,” Front. Syst. Neurosci., 13, 28 (2019), https://doi.org/10.3389/fnsys.2019.00028.
Lopez-Huerta, V. G., Denton, J. A., Nakano, Y., et al., “Striatal bilateral control of skilled forelimb movement,” Cell Rep., 34, No. 3, 108651 (2021), https://doi.org/10.1016/j.celrep.2020.108651.
Maiorov, V. I. and Serkov, A. N., “Neuron activity in the ventral tegmental area of the midbrain on fi rst performance of a conditioned active avoidance refl ex,” Zh. Vyssh. Nerv. Deyat., 66, No. 6, 725–729 (2016), 7868/S004446771606006X.
Maiorov, V. I., “A model of a neuronal mechanism of the instrumentalization of movements induced by stimulation of the motor cortex,” Zh. Vyssh. Nerv. Deyat., 71, No. 2, 202–212 (2021), https://doi.org/10.31857/S0044467721020064.
Maiorov, V. I., “Functions of dopamine in an operant conditioned refl ex,” Zh. Vyssh. Nerv. Deyat., 68, No. 4, 404–414 (2018), https://doi.org/10.1134/S0044467718040093.
Malvaez, M., “Neural substrates of habit,” J. Neurosci. Res., 98, No. 6, 986–997 (2020), https://doi.org/10.1002/jnr.24552.
Mamardashvili, M., The Esthetics of Thought. Lectures in Philosophy, Azbuka Classics, St. Petersburg (2002).
Martiros, N., Burgess, A. A., and Graybiel, A. M., “Inversely active striatal projection neurons and interneurons selectively delimit useful behavioral sequences,” Curr. Biol., 28, No. 4, 560–573.e5 (2018), https://doi.org/10.1016/j.cub.2018.01.031.
Matamales, M., McGovern, A. E., Mi, J. D., et al., “Local D2- to D1-neuron transmodulation updates goal-directed learning in the striatum,” Science, 367, No. 6477, 549–555 (2020), https://doi.org/10.1126/science.aaz5751.
Matsumoto, M. and Hikosaka, O., “Two types of dopamine neuron distinctly convey positive and negative motivational signals,” Nature, 459, 837–841 (2009), https://doi.org/10.1038/nature08028.
Mawase, F., Uehara, S., Bastian, A. J., and Celnik, P., “Motor learning enhances use-dependent plasticity,” J. Neurosci., 37, No. 10, 2673–2685 (2017), https://doi.org/10.1523/JNEUROSCI.3303-16.2017.
Menegas, W., Akiti, K., Amo, R., et al., “Dopamine neurons projecting to the posterior striatum reinforce avoidance of threatening stimuli,” Nat. Neurosci., 21, No. 10, 1421–1430 (2018), https://doi.org/10.1038/s41593-018-0222-1.
Mohebi, A., Pettibone, J. R., Hamid, A. A., et al., “Dissociable dopamine dynamics for learning and motivation,” Nature, 570, No. 7759, 65–70 (2019), https://doi.org/10.1038/s41586-019-1235-y.
Nadel, J. A., Pawelko, S. S., Copes-Finke, D., et al., “Lesion of striatal patches disrupts habitual behaviors and increases behavioral variability,” PLoS One, 15, No. 1, e0224715 (2020), https://doi.org/10.1371/journal.pone.0224715.
Nakamura, T., Nagata, M., Yagi, T., et al., “Learning new sequential stepping patterns requires striatal plasticity during the earliest phase of acquisition,” Eur. J. Neurosci., 45, No. 7, 901–911 (2017), https://doi.org/10.1111/ejn.13537.
Nakayama, H., Ibañez-Tallon, I., and Heintz, N., “Cell-type-specific contributions of medial prefrontal neurons to fl exible behaviors,” J. Neurosci., 38, No. 19, 4490–4504 (2018), https://doi.org/10.1523/JNEUROSCI.3537-17.2018.
Nisanov, R., Schelbaum, E., Morris, D., and Ranaldi, R., “CaMKII antagonism in the ventral tegmental area impairs acquisition of conditioned approach learning in rats,” Neurobiol. Learn. Mem., 175, 107299 (2020), https://doi.org/10.1016/j.nlm.2020.107299.
Nonomura, S., Nishizawa, K., Sakai, Y., et al., “Monitoring and updating of action selection for goal-directed behavior through the striatal direct and indirect pathways,” Neuron, 99, No. 6, 1302–1314.e5 (2018), https://doi.org/10.1016/j.neuron.2018.08.002.
O’Hare, J. K., Ade, K. K., Sukharnikova, T., et al., “Pathway-specifi c striatal substrates for habitual behavior,” Neuron, 89, No. 3, 472–9 (2016), https://doi.org/10.1016/j.neuron.2015.12.032.
Oldenburg, I. A. and Sabatini, B. L., “Antagonistic but not symmetric regulation of primary motor cortex by basal ganglia direct and indirect pathways,” Neuron, 86, No. 5, 1174–81 (2015), https://doi.org/10.1016/j.neuron.2015.05.008.
Oleson, E. B., Gentry, R. N., Chioma, V. C., and Cheer, J. F., “Subsecond dopamine release in the nucleus accumbens predicts conditioned punishment and its successful avoidance,” J. Neurosci., 32, No. 42, 14804–8 (2012), https://doi.org/10.1523/JNEUROSCI.3087-12.2012.
Owesson-White, C., Belle, A. M., Herr, N. R., et al., “Cue-evoked dopamine release rapidly modulates d2 neurons in the nucleus accumbens during motivated behavior,” J. Neurosci., 36, No. 22, 6011–21 (2016), https://doi.org/10.1523/JNEUROSCI.0393-16.2016.
Packard, M. G. and McGaugh, J. L., “Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning,” Neurobiol. Learn. Mem., 65, 65–72 (1996), https://doi.org/10.1006/nlme.1996.0007.
Parker, J. G., Marshall, J. D., Ahanonu, B., et al., “Diametric neural ensemble dynamics in parkinsonian and dyskinetic states,” Nature, 557, No. 7704, 177–182 (2018), https://doi.org/10.1038/s41586-018-0090-6.
Parker, N. F., Cameron, C. M., Taliaferro, J. P., et al., “Reward and choice encoding in terminals of midbrain dopamine neurons depends on striatal target,” Nat. Neurosci., 19, No. 6, 845–54 (2016), https://doi.org/10.1038/nn.4287.
Pasquereau, B. and Turner, R. S., “Dopamine neurons encode errors in predicting movement trigger occurrence,” J. Neurophysiol., 113, No. 4, 1110–1123 (2014).
Peak, J., Hart, G., and Balleine, B. W., “From learning to action: the integration of dorsal striatal input and output pathways in instrumental conditioning,” Eur. J. Neurosci., 49, No. 5, 658–671 (2019), https://doi.org/10.1111/ejn.13964.
Pinsard, B., Boutin, A., Gabitov, E., et al., “Consolidation alters motor sequence- specific distributed representations,” eLife, 8, e39324 (2019), https://doi.org/10.7554/eLife.39324.
Poulin, J. F., Caronia, G., Hofer, C., et al., “Mapping projections of molecularly defined dopamine neuron subtypes using intersectional genetic approaches,” Nat. Neurosci., 21, No. 9, 1260–1271 (2018), https://doi.org/10.1038/s41593-018-0203-4.
Reig, R. and Silberberg, G., “Multisensory integration in the mouse striatum,” Neuron, 83, No. 5, 1200–12 (2014), https://doi.org/10.1016/j.neuron.2014.07.033.
Richfield, E. K., Penney, J. B., and Young, A. B., “Anatomical and affinity state comparisons between dopamine D1 and D2 receptors in the rat central nervous system,” Neuroscience, 30, No. 3, 767–777 (1989).
Rothwell, P. E., Hayton, S. J., Sun, G. L., et al., “Input- and output-specific regulation of serial order performance by corticostriatal circuits,” Neuron, 88, No. 2, 345–56 (2015), https://doi.org/10.1016/j.neuron.2015.09.035.
Rueda-Orozco, P. E. and Robbe, D., “The striatum multiplexes contextual and kinematic information to constrain motor habits execution,” Nat. Neurosci., 18, No. 3, 453–60 (2015), https://doi.org/10.1038/nn.3924.
Sales-Carbonell, C., Taouali, W., Khalki, L., et al., “No discrete start/stop signals in the dorsal striatum of mice performing a learned action,” Curr. Biol., 28, No. 19, 3044–3055.e5 (2018), https://doi.org/10.1016/j.cub.2018.07.038.
Saund, J., Dautan, D., Rostron, C., et al., “Thalamic inputs to dorsomedial striatum are involved in inhibitory control: evidence from the five-choice serial reaction time task in rats,” Psychopharmacology (Berlin), 234, No. 16, 2399–2407 (2017), https://doi.org/10.1007/s00213-017-4627-4.
Saunders, B. T., Richard, J. M., Margolis, E. B., and Janak, P. H., “Dopamine neurons create Pavlovian conditioned stimuli with circuit-defi ned motivational properties,” Nat. Neurosci., 21, No. 8, 1072–1083 (2018), https://doi.org/10.1038/s41593-018-0191-4.
Schiff, N. D., Giacino, J. T., Kalmar, K., et al., “Behavioural improvements with thalamic stimulation after severe traumatic brain injury,” Nature, 448, No. 7153, 600–3 (2007), https://doi.org/10.1038/nature06041.
Schreiner, D. C., Renteria, R., and Gremel, C. M., “Fractionating the all-ornothing definition of goal-directed and habitual decision-making,” J. Neurosci. Res., 98, No. 6, 998–1006 (2020), https://doi.org/10.1002/jnr.24545.
Schultz, W., “Updating dopamine reward signals,” Curr. Opin. Neurobiol., 23, No. 2, 229–238 (2013).
Schultz, W., Ruffi eux, A., and Aebischer, P., “The activity of pars compacta neurons of the monkey substantia nigra in relation to motor activation,” Exp. Brain Res., 51, 377–387 (1983).
Shan, Q., Ge, M., Christie, M. J., and Balleine, B. W., “The acquisition of goal-directed actions generates opposing plasticity in direct and indirect pathways in dorsomedial striatum,” J. Neurosci., 34, 9196–9201 (2014).
Shapovalova, K. B., Pominova, E. V., and Dyubkacheva, T. A., “Characteristics of the influence of the cholinergic system of the rat neostriatum on learning active avoidance in health and disruption of the intralaminar nuclei of the thalamus,” Ros. Fiziol. Zh., 82, No. 1, 1–12 (1996).
Shen, W., Flajolet, M., Greengard, P., and Surmeier, D. J., “Dichotomous dopaminergic control of striatal synaptic plasticity,” Science, 321, No. 5890, 848–851 (2008), https://doi.org/10.1126/science.1160575.
Sheng, M. J., Lu, D., Shen, Z. M., and Poo, M. M., “Emergence of stable striatal D1R and D2R neuronal ensembles with distinct fi ring sequence during motor learning,” Proc. Natl. Acad. Sci. USA, 116, No. 22, 11038–11047 (2019), https://doi.org/10.1073/pnas.1901712116.
Shin, J. H., Kim, D., and Jung, M. W., “Differential coding of reward and movement information in the dorsomedial striatal direct and indirect pathways,” Nat. Commun., 9, No. 1, 404 (2018), https://doi.org/10.1038/s41467-017-02817-1.
Shin, J. H., Song, M., Paik, S. B., and Jung, M. W., “Spatial organization of functional clusters representing reward and movement information in the striatal direct and indirect pathways,” Proc. Natl. Acad. Sci. USA, 117, No. 43, 27004–27015 (2020), https://doi.org/10.1073/pnas.2010361117.
Sigurdsson, H. P., Jackson, S. R., Kim, S., et al., “A feasibility study for somatomotor cortical mapping in Tourette syndrome using neuronavigated transcranial magnetic stimulation,” Cortex, 129, 175–187 (2020), https://doi.org/10.1016/j.cortex.2020.04.014.
Simmons, D. V., Higgs, M. H., Lebby, S., and Wilson, C. J., “Indirect pathway control of fi ring rate and pattern in the substantia nigra pars reticulata,” J. Neurophysiol., 123, No. 2, 800–814 (2020), https://doi.org/10.1152/jn.00678.2019.
Sippy, T., Lapray, D., Crochet, S., and Petersen, C. C., “Cell-type-specific sensorimotor processing in striatal projection neurons during goal-directed behavior,” Neuron, 88, No. 2, 298–305 (2015), https://doi.org/10.1016/j.neuron.2015.08.039.
Smith, K. S. and Graybiel, A. M., “A dual operator view of habitual behavior reflecting cortical and striatal dynamics,” Neuron, 79, No. 2, 361–74 (2013), https://doi.org/10.1016/j.neuron.2013.05.038.
Sommer, W. H., Costa, R. M., and Hansson, A. C., “Dopamine systems adaptation during acquisition and consolidation of a skill,” Front. Integr. Neurosci., 8, 87 (2014), https://doi.org/10.3389/fnint.2014.00087.
Steinberg, E. E., Keifl in, R., Boivin, J. R., et al., “A causal link between prediction errors, dopamine neurons and learning,” Nat. Neurosci., 16, No. 7, 966–973 (2013), https://doi.org/10.1038/nn.3413.
Syed, E. C., Grima, L. L., Magill, P. J., et al., “Action initiation shapes mesolimbic dopamine encoding of future rewards,” Nat. Neurosci., 19, No. 1, 34–36 (2016), https://doi.org/10.1038/nn.4187.
Tecuapetla, F., Jin, X., Lima, S. Q., and Costa, R. M., “Complementary contributions of striatal projection pathways to action initiation and execution,” Cell, 166, No. 3, 703–715 (2016), https://doi.org/10.1016/j.cell.2016.06.032.
Threlfell, S., Lalic, T., Platt, N. J., et al., “Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons,” Neuron, 75, No. 1, 58–64 (2012), https://doi.org/10.1016/j.neuron.2012.04.038.
Thura, D. and Cisek, P., “The basal ganglia do not select reach targets but control the urgency of commitment,” Neuron, 95, No. 5, 1160–1170. e5 (2017), https://doi.org/10.1016/j.neuron.2017.07.039.
Tye, K. M., Mirzabekov, J. J., Warden, M. R., et al., “Dopamine neurons modulate neural encoding and expression of depression-related behavior,” Nature, 493, No. 7433, 537–541 (2013), https://doi.org/10.1038/nature11740.
Ueda, Y., Yamanaka, K., Noritake, A., et al., “Distinct functions of the primate putamen direct and indirect pathways in adaptive outcomebased action selection,” Front. Neuroanat., 11, 66 (2017), https://doi.org/10.3389/fnana.2017.00066.
Vandaele, Y., Mahajan, N. R., Ottenheimer, D. J., et al., “Distinct recruitment of dorsomedial and dorsolateral striatum erodes with extended training,” eLife, 8, e49536 (2019), https://doi.org/10.7554/eLife.49536.
Vicente, A. M., Galvão-Ferreira, P., Tecuapetla, F., and Costa, R. M., “Direct and indirect dorsolateral striatum pathways reinforce different action strategies,” Curr. Biol., 26, No. 7, R267–9 (2016), https://doi.org/10.1016/j.cub.2016.02.036.
Wang, Y., Qin, Y., Li, H., et al., “The modulation of reward and habit systems by acupuncture in adolescents with internet addiction,” Neural Plast., 2020, 7409417 (2020), https://doi.org/10.1155/2020/7409417.
Watabe-Uchida, M., Eshel, N., and Uchida, N., “Neural circuitry of reward prediction Error,” Annu. Rev. Neurosci., 40, 373–394 (2017).
Xiao, L., Chattree, G., Oscos, F. G., et al., “A basal ganglia circuit sufficient to guide birdsong learning,” Neuron, 98, No. 1, 208–221.e5 (2018), https://doi.org/10.1016/j.neuron.2018.02.020.
Xiao, X., Deng, H., Furlan, A., et al., “A genetically defi ned compartmentalized striatal direct pathway for negative reinforcement,” Cell, 183, No. 1, 211–227.e20 (2020), https://doi.org/10.1016/j.cell.2020.08.032.
Yagishita, S., Hayashi-Takagi, A., Ellis-Davies, G. C. R., et al., “A critical time window for dopamine actions on the structural plasticity of dendritic spines,” Science, 345, 1616–1620 (2014).
Yapo, C., Nair, A. G., Clement, L., et al., “Detection of phasic dopamine by D1 and D2 striatal medium spiny neurons,” J. Physiol., 595, No. 24, 7451–7475 (2017), https://doi.org/10.1113/JP274475.
Yasuda, M. and Hikosaka, O., “Functional territories in primate substantia nigra pars reticulata separately signaling stable and fl exible values,” J. Neurophysiol., 113, No. 6, 1681–96 (2015), https://doi.org/10.1152/jn.00674.2014.
Yin, H. H. and Knowlton, B. J., “The role of the basal ganglia in habit formation,” Nat. Rev. Neurosci., 7, No. 6, 464–476 (2006), https://doi.org/10.1038/nrn1919.
Yin, H. H., Mulcare, S. P., Hilário, M. R., et al., “Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill,” Nat. Neurosci., 12, No. 3, 333–41 (2009), https://doi.org/10.1038/nn.2261.
Yttri, E. A. and Dudman, J. T., “Opponent and bidirectional control of movement velocity in the basal ganglia,” Nature, 533, No. 7603, 402–6 (2016), https://doi.org/10.1038/nature17639.
Yu, X., Chen, S., and Shan, Q., “Depression in the direct pathway of the dorsomedial striatum permits the formation of habitual action,” Cereb. Cortex, 31, No. 7, 3551–3564 (2021), https://doi.org/10.1093/cercor/bhab031.
Author information
Authors and Affiliations
Corresponding author
Additional information
Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 72, No. 2, pp. 159–186, March–April, 2022.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ivlieva, N.Y. The Role of the Striatum in Motor Learning. Neurosci Behav Physi 52, 1218–1236 (2022). https://doi.org/10.1007/s11055-023-01351-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11055-023-01351-6