Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Human representation of visuo-motor uncertainty as mixtures of orthogonal basis distributions

Abstract

In many laboratory visuo-motor decision tasks, subjects compensate for their own visuo-motor error, earning close to the maximum reward possible. To do so, they must combine information about the distribution of possible error with values associated with different movement outcomes. The optimal solution is a potentially difficult computation that presupposes knowledge of the probability density function (pdf) of visuo-motor error associated with each possible planned movement. It is unclear how the brain represents such pdfs or computes with them. In three experiments, we used a forced-choice method to reveal subjects' internal representations of their spatial visuo-motor error in a speeded reaching movement. Although subjects' objective distributions were unimodal, close to Gaussian, their estimated internal pdfs were typically multimodal and were better described as mixtures of a small number of distributions differing only in location and scale. Mixtures of a small number of uniform distributions outperformed other mixture distributions, including mixtures of Gaussians.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Computation of expected gain.
Figure 2: Task and design of experiment 1.
Figure 3: Internal pdfs in the choice task of experiment 1.
Figure 4: Model fits of all subjects' internal pdfs in experiment 1.
Figure 5: Experiment 2.
Figure 6: Experiment 3.
Figure 7: U-mix simulation for ref. 31.

Similar content being viewed by others

References

  1. Bach, D.R. & Dolan, R.J. Knowing how much you don't know: a neural organization of uncertainty estimates. Nat. Rev. Neurosci. 13, 572–586 (2012).

    Article  CAS  Google Scholar 

  2. Maloney, L.T. & Zhang, H. Decision-theoretic models of visual perception and action. Vision Res. 50, 2362–2374 (2010).

    Article  Google Scholar 

  3. Trommershäuser, J., Maloney, L.T. & Landy, M.S. Decision making, movement planning and statistical decision theory. Trends Cogn. Sci. 12, 291–297 (2008).

    Article  Google Scholar 

  4. Battaglia, P.W. & Schrater, P.R. Humans trade off viewing time and movement duration to improve visuomotor accuracy in a fast reaching task. J. Neurosci. 27, 6984–6994 (2007).

    Article  CAS  Google Scholar 

  5. Faisal, A.A. & Wolpert, D.M. Near optimal combination of sensory and motor uncertainty in time during a naturalistic perception-action task. J. Neurophysiol. 101, 1901–1912 (2009).

    Article  Google Scholar 

  6. Hudson, T.E., Maloney, L.T. & Landy, M.S. Optimal compensation for temporal uncertainty in movement planning. PLOS Comput. Biol. 4, e1000130 (2008).

    Article  Google Scholar 

  7. Körding, K.P. & Wolpert, D.M. Bayesian integration in sensorimotor learning. Nature 427, 244–247 (2004).

    Article  Google Scholar 

  8. Trommershäuser, J., Maloney, L.T. & Landy, M.S. Statistical decision theory and trade-offs in the control of motor response. Spat. Vis. 16, 255–275 (2003).

    Article  Google Scholar 

  9. Jazayeri, M. & Shadlen, M.N. Temporal context calibrates interval timing. Nat. Neurosci. 13, 1020–1026 (2010).

    Article  CAS  Google Scholar 

  10. Wei, K. & Körding, K. Uncertainty of feedback and state estimation determines the speed of motor adaptation. Front. Comput. Neurosci. 4, 11 (2010).

    PubMed  PubMed Central  Google Scholar 

  11. Trommershäuser, J., Landy, M.S. & Maloney, L.T. Humans rapidly estimate expected gain in movement planning. Psychol. Sci. 17, 981–988 (2006).

    Article  Google Scholar 

  12. Ma, W.J., Beck, J.M., Latham, P.E. & Pouget, A. Bayesian inference with probabilistic population codes. Nat. Neurosci. 9, 1432–1438 (2006).

    Article  CAS  Google Scholar 

  13. Huys, Q.J., Zemel, R.S., Natarajan, R. & Dayan, P. Fast population coding. Neural Comput. 19, 404–441 (2007).

    Article  Google Scholar 

  14. Pouget, A., Beck, J.M., Ma, W.J. & Latham, P.E. Probabilistic brains: knowns and unknowns. Nat. Neurosci. 16, 1170–1178 (2013).

    Article  CAS  Google Scholar 

  15. Maloney, L.T. Statistical decision theory and biological vision. in Perception and the Physical World: Psychological and Philosophical Issues in Perception (eds. D. Heyer & R. Mausfeld) 145–189 (Wiley, New York, 2002).

  16. Haruno, M., Wolpert, D.M. & Kawato, M. Hierarchical MOSAIC for movement generation. Int. Congr. Ser. 1250, 575–590 (2003).

    Article  Google Scholar 

  17. Maloney, L.T. & Mamassian, P. Bayesian decision theory as a model of human visual perception: testing Bayesian transfer. Vis. Neurosci. 26, 147–155 (2009).

    Article  Google Scholar 

  18. Akaike, H. A new look at the statistical model identification. IEEE Trans. Automat. Contr. 19, 716–723 (1974).

    Article  Google Scholar 

  19. Hurvich, C.M. & Tsai, C.-L. Regression and time series model selection in small samples. Biometrika 76, 297–307 (1989).

    Article  Google Scholar 

  20. Stephan, K.E., Penny, W.D., Daunizeau, J., Moran, R.J. & Friston, K.J. Bayesian model selection for group studies. Neuroimage 46, 1004–1017 (2009).

    Article  Google Scholar 

  21. Zhang, H., Daw, N.D. & Maloney, L.T. Testing whether humans have an accurate model of their own motor uncertainty in a speeded reaching task. PLOS Comput. Biol. 9, e1003080 (2013).

    Article  CAS  Google Scholar 

  22. Oruç, I., Maloney, L.T. & Landy, M.S. Weighted linear cue combination with possibly correlated error. Vision Res. 43, 2451–2468 (2003).

    Article  Google Scholar 

  23. Acerbi, L., Wolpert, D.M. & Vijayakumar, S. Internal representations of temporal statistics and feedback calibrate motor-sensory interval timing. PLOS Comput. Biol. 8, e1002771 (2012).

    Article  CAS  Google Scholar 

  24. Daw, N.D., Courville, A.C. & Dayan, P. Semi-rational models of conditioning: the case of trial order. in The Probabilistic Mind: Prospects for Bayesian Cognitive Science (eds. N. Chater & M. Oaksford) 431–452 (Oxford University Press, Oxford, 2008).

  25. Gershman, S. & Wilson, R. The neural costs of optimal control. Adv. Neural Inf. Process. Syst. 23, 712–720 (2010).

    Google Scholar 

  26. Vul, E., Goodman, N.D., Griffiths, T.L. & Tenenbaum, J.B. One and done? Optimal decisions from very few samples. Cogn. Sci. 38, 599–637 (2014).

    Article  Google Scholar 

  27. Sanborn, A.N., Griffiths, T.L. & Navarro, D.J. Rational approximations to rational models: alternative algorithms for category learning. Psychol. Rev. 117, 1144 (2010).

    Article  Google Scholar 

  28. Vul, E., Hanus, D. & Kanwisher, N. Attention as inference: selection is probabilistic; responses are all-or-none samples. J. Exp. Psychol. Gen. 138, 546–560 (2009).

    Article  Google Scholar 

  29. Daw, N.D. & Courville, A. The pigeon as particle filter. in Advances in Neural Information Processing Systems (ed. J.C. Platt, D. Koller, Y. Singer & S. Roweis) 369–376 (MIT Press, 2007).

  30. Maloney, L.T. Evaluation of linear models of surface spectral reflectance with small numbers of parameters. J. Opt. Soc. Am. A 3, 1673–1683 (1986).

    Article  CAS  Google Scholar 

  31. Körding, K.P. & Wolpert, D.M. The loss function of sensorimotor learning. Proc. Natl. Acad. Sci. USA 101, 9839–9842 (2004).

    Article  Google Scholar 

  32. Todorov, E. & Jordan, M.I. Optimal feedback control as a theory of motor coordination. Nat. Neurosci. 5, 1226–1235 (2002).

    Article  CAS  Google Scholar 

  33. Harris, C.M. & Wolpert, D.M. Signal-dependent noise determines motor planning. Nature 394, 780–784 (1998).

    Article  CAS  Google Scholar 

  34. Wolpert, D.M., Ghahramani, Z. & Jordan, M.I. An internal model for sensorimotor integration. Science 269, 1880–1882 (1995).

    Article  CAS  Google Scholar 

  35. Hamilton, B.H. Does entrepreneurship pay? An empirical analysis of the returns to self-employment. J. Polit. Econ. 108, 604–631 (2000).

    Article  Google Scholar 

  36. Harvey, C.R. & Siddique, A. Conditional skewness in asset pricing tests. J. Finance 55, 1263–1295 (2000).

    Article  Google Scholar 

  37. Kraus, A. & Litzenberger, R.H. Skewness preference and the valuation of risk assets. J. Finance 31, 1085–1100 (1976).

    Google Scholar 

  38. Moskowitz, T.J. & Vissing-Jørgensen, A. The returns to entrepreneurial investment: a private equity premium puzzle? Am. Econ. Rev. 92, 745–778 (2002).

    Article  Google Scholar 

  39. Pelli, D.G. The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat. Vis. 10, 437–442 (1997).

    Article  CAS  Google Scholar 

  40. Brainard, D.H. The psychophysics toolbox. Spat. Vis. 10, 433–436 (1997).

    Article  CAS  Google Scholar 

  41. Erev, I. et al. A choice prediction competition: choices from experience and from description. J. Behav. Decis. Mak. 23, 15–47 (2010).

    Article  Google Scholar 

  42. Rasmussen, C.E. & Williams, C.K.I. Gaussian Processes for Machine Learning (MIT Press, 2006).

Download references

Acknowledgements

The authors would like to thank J. Tee for inspiring discussions. H.Z. and L.T.M. were supported by grant EY019889 from the US National Institutes of Health and L.T.M. by an award from the Alexander v. Humboldt Foundation. N.D.D. was supported by a Scholar Award from the McKnight Foundation and a James S. McDonnell Foundation Award in Understanding Human Cognition.

Author information

Authors and Affiliations

Authors

Contributions

H.Z. designed and performed the experiments, analyzed the data and wrote the manuscript. N.D.D. and L.T.M. supervised the project and improved the manuscript.

Corresponding author

Correspondence to Hang Zhang.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Visualization of subjects’ internal pdfs in Experiment 1.

Each panel is for one subject. Shaded regions denote ±SEM. is in the unit of the subject’s horizontal standard deviation estimated from the reaching task.

Supplementary Figure 2 Equivalent ratio as a function of Triple Number in Experiment 1.

Each panel is for one subject. In the choice task, there were 12 different Triples, whose paired Singles were adjusted in width by adaptive procedures (Fig. 2e). For each subject and each Triple, we defined the equivalent width of a Triple as the width of the Single that the subject judged to be as “hittable” as the Triple. We defined the equivalent ratio as the ratio of the equivalent width of the Triple to the total width of its three rectangles. The equivalent ratio provides a measure for the probability density function in subjects’ internal pdf, roughly indicating the mean probability density over the side rectangles of the Triple relative to the probability density around the center. The 12 Triples in the plot are sorted by the horizontal position of the right rectangle in the Triple. Note the measured equivalent ratios (black dots and line) had abrupt changes at adjacent Triples. The U-mix prediction (green line) captured the abrupt changes better than the predictions of the Gaussian prediction (blue line). The predictions of other mixture models (especially mG-mix) were close to that of U-mix and were omitted in the plot for simplicity.

Supplementary Figure 3 Visualization of subjects’ internal pdfs in Experiment 2.

Each panel is for one subject. Shaded regions denote ±SEM. is in the unit of the subject’s vertical standard deviation estimated from the reaching task.

Supplementary Figure 4 Model fits of subjects’ internal pdfs in Experiment 2.

(a) mG-mix model. (b) U-mix model. Each panel is for the probability density function of one subject. is in the unit of the subject’s vertical standard deviation estimated from the reaching task. Subjects are in the same order as in Supplementary Figure 3.

Supplementary Figure 5 Model fits of subjects’ internal pdfs in Experiment 3 for the mG-mix model.

Each panel is for one subject. The pair of numbers inside each panel denotes the numbers of components for the horizontal and vertical directions. Green and gray curves respectively denote probability density functions in the horizontal and vertical directions. is in the unit of the subject’s standard deviation (averaged across the horizontal and vertical directions) estimated from the reaching task.

Supplementary Figure 6 Model fits of subjects’ internal pdfs in Experiment 3 for the U-mix model.

Each panel is for one subject. The pair of numbers inside each panel denotes the numbers of components for the horizontal and vertical directions. Green and gray curves respectively denote probability density functions in the horizontal and vertical directions. is in the unit of the subject’s standard deviation (averaged across the horizontal and vertical directions) estimated from the reaching task. Subjects are in the same order as in Supplementary Figure 5.

Supplementary Figure 7 mG-mix simulation for Körding and Wolpert31.

Similar to Figure 7, except that the U-mix representation was replaced by an mG-mix representation (Methods online). (a) Illustration of the mG-mix representation. (b) Simulated aim points vs. data.

Supplementary information

Source data

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, H., Daw, N. & Maloney, L. Human representation of visuo-motor uncertainty as mixtures of orthogonal basis distributions. Nat Neurosci 18, 1152–1158 (2015). https://doi.org/10.1038/nn.4055

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.4055

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing