Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-22T22:26:13.895Z Has data issue: false hasContentIssue false
  • English
  • Français

Reducing behavioral dimensions to study brain–environment interactions

Published online by Cambridge University Press:  30 September 2021

David Thura Open the ORCID record for David Thura [Opens in a new window]
David Thura*
Affiliation:
Lyon Neuroscience Research Center – ImpAct team, Inserm U1028 – CNRS UMR5292 – Lyon 1 University, 69676Bron, France. [email protected]; davidthura.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Movement vigor provides a window on action valuation. But what is vigor, and how to measure it in the first place? Strikingly, many different co-varying vigor-related metrics can be found in the literature. I believe this is because vigor, just like the neural circuits that determine it, is an integrated, low-dimensional parameter. As such, it can only be roughly estimated.

Type
Open Peer Commentary
Information
Behavioral and Brain Sciences , Volume 44 , 2021 , e135
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Baker, B., Lansdell, B., & Kording, K. (2021). A philosophical understanding of representation for neuroscience. ArXiv:2102.06592, 15.Google Scholar
Ballesta, S., Shi, W., Conen, K. E., & Padoa-Schioppa, C. (2020). Values encoded in orbitofrontal cortex are causally related to economic choices. Nature, 588(7838), 450–453. https://doi.org/10.1038/s41586-020-2880-x.CrossRefGoogle ScholarPubMed
Baraduc, P., Thobois, S., Gan, J., Broussolle, E., & Desmurget, M. (2013). A common optimization principle for motor execution in healthy subjects and Parkinsonian patients. Journal of Neuroscience, 33(2), 665–677. https://doi.org/10.1523/JNEUROSCI.1482-12.2013.CrossRefGoogle ScholarPubMed
Berger, M., Agha, N. S., & Gail, A. (2020). Wireless recording from unrestrained monkeys reveals motor goal encoding beyond immediate reach in frontoparietal cortex. eLife, 9, e51322. https://doi.org/10.7554/eLife.51322.CrossRefGoogle ScholarPubMed
Berret, B., Castanier, C., Bastide, S., & Deroche, T. (2018). Vigour of self-paced reaching movement: Cost of time and individual traits. Scientific Reports, 8(1), 10655. https://doi.org/10.1038/s41598-018-28979-6.CrossRefGoogle ScholarPubMed
Brette, R. (2019). Is coding a relevant metaphor for the brain? Behavioral and Brain Sciences, 42, e215. https://doi.org/10.1017/S0140525X19000049.CrossRefGoogle Scholar
Buzsáki, G. (2019). The brain from inside out. Oxford University Press.CrossRefGoogle Scholar
Choi, J. E. S., Vaswani, P. A., & Shadmehr, R. (2014). Vigor of movements and the cost of time in decision making. Journal of Neuroscience, 34(4), 1212–1223. https://doi.org/10.1523/JNEUROSCI.2798-13.2014.CrossRefGoogle ScholarPubMed
Cisek, P. (1999). Beyond the computer metaphor: Behaviour as interaction. Journal of Consciousness Studies, 6(11–12), 125–142.Google Scholar
Cisek, P. (2007). Cortical mechanisms of action selection: The affordance competition hypothesis. Philosophical Transactions of the Royal Society B: Biological Sciences, 362(1485), 1585–1599. https://doi.org/10.1098/rstb.2007.2054.CrossRefGoogle ScholarPubMed
Cisek, P. (2019). Resynthesizing behavior through phylogenetic refinement. Attention, Perception, & Psychophysics, 81(7), 2265–2287. https://doi.org/10.3758/s13414-019-01760-1.CrossRefGoogle ScholarPubMed
Cisek, P., & Kalaska, J. F. (2010). Neural mechanisms for interacting with a world full of action choices. Annual Review of Neuroscience, 33(1), 269–298. https://doi.org/10.1146/annurev.neuro.051508.135409.CrossRefGoogle ScholarPubMed
Cisek, P., & Thura, D. (2018). Neural circuits for action selection. In Corbetta, D. & Santello, M. (Eds.), Reach-to-grasp behavior: Brain, behavior, and modelling across the life span (pp. 91–118). Taylor & Francis Group.CrossRefGoogle Scholar
Collins, A. G. E., & Frank, M. J. (2016). Surprise! Dopamine signals mix action, value and error. Nature Neuroscience, 19(1), 3–5. https://doi.org/10.1038/nn.4207.CrossRefGoogle Scholar
da Silva, J. A., Tecuapetla, F., Paixão, V., & Costa, R. M. (2018). Dopamine neuron activity before action initiation gates and invigorates future movements. Nature, 554(7691), 244–248. https://doi.org/10.1038/nature25457.CrossRefGoogle ScholarPubMed
Dezfouli, A., Balleine, B. W., & Nock, R. (2019). Optimal response vigor and choice under non-stationary outcome values. Psychonomic Bulletin & Review, 26(1), 182–204. https://doi.org/10.3758/s13423-018-1500-3.CrossRefGoogle ScholarPubMed
Dombeck, D. A., & Reiser, M. B. (2012). Real neuroscience in virtual worlds. Current Opinion in Neurobiology, 22(1), 3–10. https://doi.org/10.1016/j.conb.2011.10.015.CrossRefGoogle ScholarPubMed
Gigerenzer, G., & Gaissmaier, W. (2011). Heuristic decision making. Annual Review of Psychology, 62(1), 451–482. https://doi.org/10.1146/annurev-psych-120709-145346.CrossRefGoogle ScholarPubMed
Glimcher, P. W., Dorris, M. C., & Bayer, H. M. (2005). Physiological utility theory and the neuroeconomics of choice. Games and Economic Behavior, 52(2), 213–256. https://doi.org/10.1016/j.geb.2004.06.011.CrossRefGoogle ScholarPubMed
Gomez-Marin, A., & Ghazanfar, A. A. (2019). The life of behavior. Neuron, 104(1), 25–36. https://doi.org/10.1016/j.neuron.2019.09.017.CrossRefGoogle ScholarPubMed
Graziano, M. (2006). The organization of behavioral repertoire in motor cortex. Annual Review of Neuroscience, 29(1), 105–134. https://doi.org/10.1146/annurev.neuro.29.051605.112924.CrossRefGoogle ScholarPubMed
Griffiths, B., & Beierholm, U. R. (2017). Opposing effects of reward and punishment on human vigor. Scientific Reports, 7(1), 42287. https://doi.org/10.1038/srep42287.CrossRefGoogle ScholarPubMed
Grillner, S., & Robertson, B. (2016). The basal ganglia over 500 million years. Current Biology, 26(20), R1088–R1100. https://doi.org/10.1016/j.cub.2016.06.041.CrossRefGoogle ScholarPubMed
Guitart-Masip, M., Beierholm, U. R., Dolan, R., Duzel, E., & Dayan, P. (2011). Vigor in the face of fluctuating rates of reward: An experimental examination. Journal of Cognitive Neuroscience, 23(12), 3933–3938. https://doi.org/10.1162/jocn_a_00090.CrossRefGoogle Scholar
Hayden, B. Y., & Niv, Y. (2020). The case against economic values in the brain. PsyArXiv Preprints. https://doi.org/10.31234/osf.io/7hgup.CrossRefGoogle Scholar
Humphries, M. D. (2020). Strong and weak principles of neural dimension reduction. ArXiv:2011.08088 [q-Bio]. http://arxiv.org/abs/2011.08088.Google Scholar
Jourjine, N., & Hoekstra, H. E. (2021). Expanding evolutionary neuroscience: Insights from comparing variation in behavior. Neuron, 109(7), 1084–1099. https://doi.org/10.1016/j.neuron.2021.02.002.CrossRefGoogle ScholarPubMed
Jurado-Parras, M.-T., Safaie, M., Sarno, S., Louis, J., Karoutchi, C., Berret, B., & Robbe, D. (2020). The dorsal striatum energizes motor routines. Current Biology, 16; 30(22), 4362–4372, e6. https://doi.org/10.1016/j.cub.2020.08.049.CrossRefGoogle ScholarPubMed
Kalaska, J. F. (2009). From intention to action: Motor Cortex and the control of reaching movements. In Sternad, D. (Ed.), Progress in motor control (Vol. 629, pp. 139–178). Springer US. https://doi.org/10.1007/978-0-387-77064-2_8.CrossRefGoogle Scholar
Kalaska, JF (2019). Emerging ideas and tools to study the emergent properties of the cortical neural circuits for voluntary motor control in non-human primates. F1000Research, 8(F1000 Faculty Rev):749. https://doi.org/10.12688/f1000research.17161.1.CrossRefGoogle Scholar
Katz, P. S. (2016). Evolution of central pattern generators and rhythmic behaviours. Philosophical Transactions of the Royal Society B: Biological Sciences, 371(1685), 20150057. https://doi.org/10.1098/rstb.2015.0057.CrossRefGoogle ScholarPubMed
Krakauer, J. W., Ghazanfar, A. A., Gomez-Marin, A., MacIver, M. A., & Poeppel, D. (2017). Neuroscience needs behavior: Correcting a reductionist bias. Neuron, 93(3), 480–490. https://doi.org/10.1016/j.neuron.2016.12.041.CrossRefGoogle ScholarPubMed
Lee, D., Seo, H., & Jung, M. W. (2012). Neural basis of reinforcement learning and decision making. Annual Review of Neuroscience, 35(1), 287–308. https://doi.org/10.1146/annurev-neuro-062111-150512.CrossRefGoogle ScholarPubMed
Mathis, A., Mamidanna, P., Cury, K. M., Abe, T., Murthy, V. N., Mathis, M. W., & Bethge, M. (2018). DeepLabCut: Markerless pose estimation of user-defined body parts with deep learning. Nature Neuroscience, 21(9), 1281–1289. https://doi.org/10.1038/s41593-018-0209-y.CrossRefGoogle ScholarPubMed
Mazzoni, P., Hristova, A., & Krakauer, J. W. (2007). Why don't we move faster? Parkinson's disease, movement vigor, and implicit motivation. Journal of Neuroscience, 27(27), 7105–7116. https://doi.org/10.1523/JNEUROSCI.0264-07.2007.CrossRefGoogle ScholarPubMed
Milstein, D. M., & Dorris, M. C. (2007). The influence of expected value on saccadic preparation. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 27(18), 4810–4818. https://doi.org/10.1523/JNEUROSCI.0577-07.2007.CrossRefGoogle ScholarPubMed
Muhammed, K., Dalmaijer, E., Manohar, S., & Husain, M. (2020). Voluntary modulation of saccadic peak velocity associated with individual differences in motivation. Cortex, 122, 198–212. https://doi.org/10.1016/j.cortex.2018.12.001.CrossRefGoogle ScholarPubMed
Niv, Y. (2020). The primacy of behavioral research for understanding the brain [Preprint]. PsyArXiv. https://doi.org/10.31234/osf.io/y8mxe.CrossRefGoogle Scholar
Niv, Y., Daw, N. D., Joel, D., & Dayan, P. (2007). Tonic dopamine: Opportunity costs and the control of response vigor. Psychopharmacology, 191(3), 507–520. https://doi.org/10.1007/s00213-006-0502-41CrossRefGoogle ScholarPubMed
Noel, J.-P., Caziot, B., Bruni, S., Fitzgerald, N. E., Avila, E., & Angelaki, D. E. (2021). Supporting generalization in non-human primate behavior by tapping into structural knowledge: Examples from sensorimotor mappings, inference, and decision-making. Progress in Neurobiology, 201:101996. doi: 10.1016/j.pneurobio.2021.101996. Epub 2021 Jan 14. PMID: 33454361; PMCID: PMC8096669. https://doi.org/10.1016/j.pneurobio.2021.101996.CrossRefGoogle ScholarPubMed
Panigrahi, B., Martin, K. A., Li, Y., Graves, A. R., Vollmer, A., Olson, L., … Dudman, J. T. (2015). Dopamine is required for the neural representation and control of movement vigor. Cell, 162(6), 1418–1430. https://doi.org/10.1016/j.cell.2015.08.014.CrossRefGoogle ScholarPubMed
Ramkumar, P., Dekleva, B., Cooler, S., Miller, L., & Kording, K. (2016). Premotor and motor cortices encode reward. PLoS ONE, 11(8), e0160851. https://doi.org/10.1371/journal.pone.0160851.CrossRefGoogle ScholarPubMed
Reimer, J., & Hatsopoulos, N. G. (2009). The problem of parametric neural coding in the motor system. Advances in Experimental Medicine and Biology, 629, 243–259. https://doi.org/10.1007/978-0-387-77064-2_12.CrossRefGoogle ScholarPubMed
Renoult, L., Roux, S., & Riehle, A. (2006). Time is a rubberband: Neuronal activity in monkey motor cortex in relation to time estimation. The European Journal of Neuroscience, 23(11), 3098–3108. https://doi.org/10.1111/j.1460-9568.2006.04824.x.CrossRefGoogle ScholarPubMed
Reppert, T. R., Lempert, K. M., Glimcher, P. W., & Shadmehr, R. (2015). Modulation of saccade vigor during value-based decision making. Journal of Neuroscience, 35(46), 15369–15378. https://doi.org/10.1523/JNEUROSCI.2621-15.2015.CrossRefGoogle ScholarPubMed
Reppert, T. R., Rigas, I., Herzfeld, D. J., Sedaghat-Nejad, E., Komogortsev, O., & Shadmehr, R. (2018). Movement vigor as a traitlike attribute of individuality. Journal of Neurophysiology, 120(2), 741–757. https://doi.org/10.1152/jn.00033.2018.CrossRefGoogle ScholarPubMed
Reynaud, A. J., Saleri Lunazzi, C., & Thura, D. (2020). Humans sacrifice decision-making for action execution when a demanding control of movement is required. Journal of Neurophysiology, 124(2), 497–509. https://doi.org/10.1152/jn.00220.2020.CrossRefGoogle ScholarPubMed
Rueda-Orozco, P. E., & Robbe, D. (2015). The striatum multiplexes contextual and kinematic information to constrain motor habits execution. Nature Neuroscience, 18(3), 453–460. https://doi.org/10.1038/nn.3924.CrossRefGoogle ScholarPubMed
Salamone, J. D., Pardo, M., Yohn, S. E., López-Cruz, L., SanMiguel, N., & Correa, M. (2016). Mesolimbic dopamine and the regulation of motivated behavior. In Simpson, E. H. & Balsam, P. D. (Eds.), Behavioral neuroscience of motivation (pp. 231–257). Springer International Publishing. https://doi.org/10.1007/7854_2015_383.Google Scholar
Saxena, S., & Cunningham, J. P. (2019). Towards the neural population doctrine. Current Opinion in Neurobiology, 55, 103–111. https://doi.org/10.1016/j.conb.2019.02.002.CrossRefGoogle ScholarPubMed
Sedaghat-Nejad, E., Herzfeld, D. J., & Shadmehr, R. (2019). Reward prediction error modulates saccade vigor. The Journal of Neuroscience, 39(25), 5010–5017. https://doi.org/10.1523/JNEUROSCI.0432-19.2019.CrossRefGoogle ScholarPubMed
Shadmehr, R., & Ahmed, A. A. (2020). Vigor: Neuroeconomics of movement control. The MIT Press. https://doi.org/10.7551/mitpress/12940.001.0001.CrossRefGoogle Scholar
Summerside, E. M., Shadmehr, R., & Ahmed, A. A. (2018). Vigor of reaching movements: Reward discounts the cost of effort. Journal of Neurophysiology, 119(6), 2347–2357. https://doi.org/10.1152/jn.00872.2017.CrossRefGoogle ScholarPubMed
Thura, D. (2020). Decision urgency invigorates movement in humans. Behavioural Brain Research, 382, 112477. https://doi.org/10.1016/j.bbr.2020.112477.CrossRefGoogle ScholarPubMed
Thura, D., & Cisek, P. (2017). The basal ganglia do not select reach targets but control the urgency of commitment. Neuron, 95(5), 1160–1170.e5. https://doi.org/10.1016/j.neuron.2017.07.039.CrossRefGoogle ScholarPubMed
Thura, D., Cos, I., Trung, J., & Cisek, P. (2014). Context-dependent urgency influences speed-accuracy trade-offs in decision-making and movement execution. The Journal of Neuroscience, 34(49), 16442–16454. https://doi.org/10.1523/JNEUROSCI.0162-14.2014.CrossRefGoogle ScholarPubMed
Turner, R. S., & Desmurget, M. (2010). Basal ganglia contributions to motor control: A vigorous tutor. Current Opinion in Neurobiology, 20(6), 704–716. https://doi.org/10.1016/j.conb.2010.08.022.CrossRefGoogle ScholarPubMed
Vyas, S., Golub, M. D., Sussillo, D., & Shenoy, K. V. (2020). Computation through neural population dynamics. Annual Review of Neuroscience, 43(1), 249–275. https://doi.org/10.1146/annurev-neuro-092619-094115.CrossRefGoogle ScholarPubMed
Yttri, E. A., & Dudman, J. T. (2016). Opponent and bidirectional control of movement velocity in the basal ganglia. Nature, 533(7603), 402–406. https://doi.org/10.1038/nature17639.CrossRefGoogle ScholarPubMed
Zenon, A., Devesse, S., & Olivier, E. (2016). Dopamine manipulation affects response vigor independently of opportunity cost. Journal of Neuroscience, 36(37), 9516–9525. https://doi.org/10.1523/JNEUROSCI.4467-15.2016.CrossRefGoogle ScholarPubMed