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.

A supramodal accumulation-to-bound signal that determines perceptual decisions in humans

Abstract

In theoretical accounts of perceptual decision-making, a decision variable integrates noisy sensory evidence and determines action through a boundary-crossing criterion. Signals bearing these very properties have been characterized in single neurons in monkeys, but have yet to be directly identified in humans. Using a gradual target detection task, we isolated a freely evolving decision variable signal in human subjects that exhibited every aspect of the dynamics observed in its single-neuron counterparts. This signal could be continuously tracked in parallel with fully dissociable sensory encoding and motor preparation signals, and could be systematically perturbed mid-flight during decision formation. Furthermore, we found that the signal was completely domain general: it exhibited the same decision-predictive dynamics regardless of sensory modality and stimulus features and tracked cumulative evidence even in the absence of overt action. These findings provide a uniquely clear view on the neural determinants of simple perceptual decisions in humans.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Distinct sensory evidence and decision signals observed during gradual target detection.
Figure 2: Decision signals determine the probability of target detection.
Figure 3: The CPP decision signal closely tracks incoming sensory evidence with temporal precision irrespective of action requirement.
Figure 4: The CPP decision signal accumulates incoming sensory evidence irrespective of sensory modality or target feature.
Figure 5: The CPP shares many of the characteristics of the classic P300 component.

Similar content being viewed by others

References

  1. Smith, P.L. & Vickers, D. The accumulator model of two-choice discrimination. J. Math. Psychol. 32, 135–168 (1988).

    Article  Google Scholar 

  2. Gold, J.I. & Shadlen, M.N. The neural basis of decision making. Annu. Rev. Neurosci. 30, 535–574 (2007).

    Article  CAS  Google Scholar 

  3. Hanes, D.P. & Schall, J.D. Neural control of voluntary movement initiation. Science 274, 427–430 (1996).

    Article  CAS  Google Scholar 

  4. Smith, P.L. & Ratcliff, R. Psychology and neurobiology of simple decisions. Trends Neurosci. 27, 161–168 (2004).

    Article  CAS  Google Scholar 

  5. Britten, K.H., Newsome, W.T., Shadlen, M.N., Celebrini, S. & Movshon, J.A. A relationship between behavioral choice and the visual responses of neurons in macaque MT. Vis. Neurosci. 13, 87–100 (1996).

    Article  CAS  Google Scholar 

  6. Parker, A.J. & Newsome, W.T. Sense and the single neuron: probing the physiology of perception. Annu. Rev. Neurosci. 21, 227–277 (1998).

    Article  CAS  Google Scholar 

  7. Romo, R. & Salinas, E. Touch and go: decision-making mechanisms in somatosensation. Annu. Rev. Neurosci. 24, 107–137 (2001).

    Article  CAS  Google Scholar 

  8. Kiani, R. & Shadlen, M.N. Representation of confidence associated with a decision by neurons in the parietal cortex. Science 324, 759–764 (2009).

    Article  CAS  Google Scholar 

  9. Kiani, R., Hanks, T.D. & Shadlen, M.N. Bounded integration in parietal cortex underlies decisions even when viewing duration is dictated by the environment. J. Neurosci. 28, 3017–3029 (2008).

    Article  CAS  Google Scholar 

  10. Shadlen, M.N. & Newsome, W.T. Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. J. Neurophysiol. 86, 1916–1936 (2001).

    Article  CAS  Google Scholar 

  11. Heekeren, H.R., Marrett, S. & Ungerleider, L.G. The neural systems that mediate human perceptual decision making. Nat. Rev. Neurosci. 9, 467–479 (2008).

    Article  CAS  Google Scholar 

  12. Philiastides, M.G., Ratcliff, R. & Sajda, P. Neural representation of task difficulty and decision making during perceptual categorization: a timing diagram. J. Neurosci. 26, 8965–8975 (2006).

    Article  CAS  Google Scholar 

  13. Ratcliff, R., Philiastides, M.G. & Sajda, P. Quality of evidence for perceptual decision making is indexed by trial-to-trial variability of the EEG. Proc. Natl. Acad. Sci. USA 106, 6539–6544 (2009).

    Article  CAS  Google Scholar 

  14. Hunt, L.T. et al. Mechanisms underlying cortical activity during value-guided choice. Nat. Neurosci. 15, 470–476 (2012).

    Article  CAS  Google Scholar 

  15. Heekeren, H.R., Marrett, S., Bandettini, P.A. & Ungerleider, L.G. A general mechanism for perceptual decision-making in the human brain. Nature 431, 859–862 (2004).

    Article  CAS  Google Scholar 

  16. Tosoni, A., Galati, G., Romani, G.L. & Corbetta, M. Sensory-motor mechanisms in human parietal cortex underlie abritrary visual decisions. Nat. Neurosci. 11, 1446–1453 (2008).

    Article  CAS  Google Scholar 

  17. Ho, T.C., Brown, S. & Serences, J.T. Domain general mechanisms of perceptual decision making in human cortex. J. Neurosci. 29, 8675–8687 (2009).

    Article  CAS  Google Scholar 

  18. Pfurtscheller, G. & Lopes da Silva, F.J. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin. Neurophysiol. 110, 1842–1857 (1999).

    Article  CAS  Google Scholar 

  19. Donner, T.H., Siegel, M., Fries, P. & Engel, A.K. Buildup of choice-predictive activity in human motor cortex during perceptual decision making. Curr. Biol. 19, 1581–1585 (2009).

    Article  CAS  Google Scholar 

  20. Di Russo, F. et al. Spatiotemporal analysis of the cortical sources of the steady-state visual evoked potential. Hum. Brain Mapp. 28, 323–334 (2007).

    Article  Google Scholar 

  21. Green, D.M. & Swets, J.A. Signal Detection Theory and Psychophysics (Wiley, New York, 1966).

  22. Nieuwenhuis, S., Aston-Jones, G. & Cohen, J.D. Decision making, the P3 and the locus coeruleus–norepinephrine system. Psychol. Bull. 131, 510–532 (2005).

    Article  Google Scholar 

  23. Huk, A.C. & Shadlen, M.N. Neural activity in macaque parietal cortex reflects temporal integration of visual motion signals during perceptual decision making. J. Neurosci. 25, 10420–10436 (2005).

    Article  CAS  Google Scholar 

  24. Cook, E.P. & Maunsell, J.H. Dynamics of neuronal responses in macaque MT and VIP during motion detection. Nat. Neurosci. 5, 985–994 (2002).

    Article  CAS  Google Scholar 

  25. Bennur, S. & Gold, J.I. Distinct representations of a perceptual decision and the associated oculomotor plan in the monkey lateral intraparietal area. J. Neurosci. 31, 913–921 (2011).

    Article  CAS  Google Scholar 

  26. Horwitz, G.D., Batista, A.P. & Newsome, W.T. Representation of an abstract perceptual decision in macaque superior colliculus. J. Neurophysiol. 91, 2281–2296 (2004).

    Article  Google Scholar 

  27. Fitzgerald, J.K., Freedman, D. & Assad, J. Generalized associative representations in parietal cortex. Nat. Neurosci. 14, 1075–1079 (2011).

    Article  CAS  Google Scholar 

  28. Rorie, A.E. & Newsome, W.T. A general mechanism for decision-making in the human brain. Trends Cogn. Sci. 9, 41–43 (2005).

    Article  Google Scholar 

  29. O'Connell, R.G. et al. Uncovering the neural signature of lapsing attention: electrophysiological signals predict errors up to 20 s before they occur. J. Neurosci. 29, 8604–8611 (2009).

    Article  CAS  Google Scholar 

  30. Polich, J. & Criado, J.R. Neuropsychology and neuropharmacology of P3a and P3b. Int. J. Psychophysiol. 60, 172–185 (2006).

    Article  Google Scholar 

  31. Woods, D.L., Hillyard, S.A., Courchesne, E. & Galambos, R. Electrophysiological signs of split-second decision-making. Science 207, 655–657 (1980).

    Article  CAS  Google Scholar 

  32. Hillyard, S.A., Squires, K.C., Bauer, J.W. & Lindsay, P.H. Evoked potential correlates of auditory signal detection. Science 172, 1357–1360 (1971).

    Article  CAS  Google Scholar 

  33. Kok, A. On the utility of P3 amplitude as a measure of processing capacity. Psychophysiology 38, 557–577 (2001).

    Article  CAS  Google Scholar 

  34. Verleger, R., Jaskowski, P. & Wascher, E. Evidence for an integrative role of P3b in linking reaction to perception. J. Psychophysiol. 19, 165–181 (2005).

    Article  Google Scholar 

  35. Donchin, E. & Coles, M.G.H. Is the P300 component a manifestation of context updating? Brain Behav. Sci. 11, 357–374 (1988).

    Article  Google Scholar 

  36. Kopp, B. The P300 component of the event-related brain potential and Bayes' theorem. Cogn. Sci. 2, 113–125 (2007).

    Google Scholar 

  37. Mars, R.B. et al. Trial-by-trial fluctuations in the event-related electroencephalogram reflect dynamic changes in the degree of surprise. J. Neurosci. 28, 12539–12545 (2008).

    Article  CAS  Google Scholar 

  38. Delorme, A. & Makeig, S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 134, 9–21 (2004).

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank S. Hillyard, I. Robertson, M. Bellgrove, E. Lalor and J. Balsters for helpful comments, and P. Collins, E. Lacey, C. Devine and D. Allen for their assistance with data collection. This work was supported by an Irish Research Council for Science Engineering and Technology EMPOWER fellowship (R.G.O.).

Author information

Authors and Affiliations

Authors

Contributions

The study was jointly conceived by R.G.O., P.M.D. and S.P.K. The experiments and tasks were designed by R.G.O. and S.P.K. S.P.K. programmed the tasks and R.G.O. collected the data. R.G.O. and S.P.K. analyzed the data and wrote the manuscript.

Corresponding author

Correspondence to Simon P Kelly.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–4 (PDF 616 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

O'Connell, R., Dockree, P. & Kelly, S. A supramodal accumulation-to-bound signal that determines perceptual decisions in humans. Nat Neurosci 15, 1729–1735 (2012). https://doi.org/10.1038/nn.3248

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.3248

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