Letter | Published:

Decision-related activity in sensory neurons reflects more than a neuron’s causal effect

Nature volume 459, pages 8992 (07 May 2009) | Download Citation

Subjects

Abstract

During perceptual decisions, the activity of sensory neurons correlates with a subject’s percept, even when the physical stimulus is identical1,2,3,4,5,6,7,8,9. The origin of this correlation is unknown. Current theory proposes a causal effect of noise in sensory neurons on perceptual decisions10,11,12, but the correlation could result from different brain states associated with the perceptual choice13 (a top-down explanation). These two schemes have very different implications for the role of sensory neurons in forming decisions14. Here we use white-noise analysis15 to measure tuning functions of V2 neurons associated with choice and simultaneously measure how the variation in the stimulus affects the subjects’ (two macaques) perceptual decisions16,17,18. In causal models, stronger effects of the stimulus upon decisions, mediated by sensory neurons, are associated with stronger choice-related activity. However, we find that over the time course of the trial these measures change in different directions—at odds with causal models. An analysis of the effect of reward size also supports this conclusion. Finally, we find that choice is associated with changes in neuronal gain that are incompatible with causal models. All three results are readily explained if choice is associated with changes in neuronal gain caused by top-down phenomena that closely resemble attention19. We conclude that top-down processes contribute to choice-related activity. Thus, even forming simple sensory decisions involves complex interactions between cognitive processes and sensory neurons.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    & Neuronal correlates of subjective visual perception. Science 245, 761–763 (1989)

  2. 2.

    & Activity changes in early visual cortex reflect monkeys’ percepts during binocular rivalry. Nature 379, 549–553 (1996)

  3. 3.

    , , , & A relationship between behavioral choice and the visual responses of neurons in macaque MT. Vis. Neurosci. 13, 87–100 (1996)

  4. 4.

    & Contribution of area MT to stereoscopic depth perception: choice-related response modulations reflect task strategy. Neuron 42, 297–310 (2004)

  5. 5.

    , , & Neural correlates of fine depth discrimination in monkey inferior temporal cortex. J. Neurosci. 25, 10796–10802 (2005)

  6. 6.

    & Macaque V2 neurons, but not V1 neurons, show choice-related activity. J. Neurosci. 26, 9567–9578 (2006)

  7. 7.

    , , & Perceptually bistable three-dimensional figures evoke high choice probabilities in cortical area MT. J. Neurosci. 21, 4809–4821 (2001)

  8. 8.

    & Neural population code for fine perceptual decisions in area MT. Nature Neurosci. 8, 99–106 (2005)

  9. 9.

    & Neuronal correlates of perception in early visual cortex. Nature Neurosci. 6, 414–420 (2003)

  10. 10.

    , , & A computational analysis of the relationship between neuronal and behavioral responses to visual motion. J. Neurosci. 16, 1486–1510 (1996)

  11. 11.

    & Probabilistic reasoning by neurons. Nature 447, 1075–1080 (2007)

  12. 12.

    Neural correlates of decision processes: neural and mental chronometry. Curr. Opin. Neurobiol. 13, 182–186 (2003)

  13. 13.

    A common neuronal code for perceptual processes in visual cortex? Comparing choice and attentional correlates in V5/MT. Phil. Trans. R. Soc. Lond. B 359, 929–941 (2004)

  14. 14.

    & Brain states: top-down influences in sensory processing. Neuron 54, 677–696 (2007)

  15. 15.

    , & Dynamics of orientation tuning in macaque primary visual cortex. Nature 387, 281–284 (1997)

  16. 16.

    , & Probing the human stereoscopic system with reverse correlation. Nature 401, 695–698 (1999)

  17. 17.

    Perceptual classification images from Vernier acuity masked by noise. Perception 26, 18 (1996)

  18. 18.

    & Psychophysically measured task strategy for disparity discrimination is reflected in V2 neurons. Nature Neurosci. 10, 1608–1614 (2007)

  19. 19.

    & Feature-based attention influences motion processing gain in macaque visual cortex. Nature 399, 575–579 (1999)

  20. 20.

    & Representation of a perceptual decision in developing oculomotor commands. Nature 404, 390–394 (2000)

  21. 21.

    & The neural basis of decision making. Annu. Rev. Neurosci. 30, 535–574 (2007)

  22. 22.

    , , & A role for neural integrators in perceptual decision making. Cereb. Cortex 13, 1257–1269 (2003)

  23. 23.

    , , & Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 273, 1868–1871 (1996)

  24. 24.

    The variability of discharge of simple cells in the cat striate cortex. Exp. Brain Res. 44, 437–440 (1981)

  25. 25.

    & Working memory in primate sensory systems. Nature Rev. Neurosci. 6, 97–107 (2005)

  26. 26.

    , , & Bayesian inference with probabilistic population codes. Nature Neurosci. 9, 1432–1438 (2006)

  27. 27.

    & Feature-based attention increases the selectivity of population responses in primate visual cortex. Curr. Biol. 14, 744–751 (2004)

  28. 28.

    & Optimal representation of sensory information by neural populations. Nature Neurosci. 9, 690–696 (2006)

  29. 29.

    , , & Stable perception of visually ambiguous patterns. Nature Neurosci. 5, 605–609 (2002)

  30. 30.

    & Binocular neurons in V1 of awake monkeys are selective for absolute, not relative, disparity. J. Neurosci. 19, 5602–5618 (1999)

  31. 31.

    , & Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res. 20, 535–538 (1980)

Download references

Acknowledgements

This research was supported by the Intramural Research Program of the US National Institutes of Health, National Eye Institute. We are grateful to J. A. Movshon and M. Shadlen for discussions and to the members of the Laboratory of Sensorimotor Research for comments on an earlier version of this manuscript. We also thank D. Parker and B. Nagy for excellent animal care.

Author Contributions H.N. designed the project, collected the data, performed the analyses and wrote the paper. B.G.C. supervised the project.

Author information

Affiliations

  1. Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, 49 Convent Drive, Bethesda, Maryland 20892, USA

    • Hendrikje Nienborg
    •  & Bruce G. Cumming

Authors

  1. Search for Hendrikje Nienborg in:

  2. Search for Bruce G. Cumming in:

Corresponding author

Correspondence to Hendrikje Nienborg.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Methods and Results, a Supplementary Discussion, Supplementary References and Supplementary Figures 1-6 with Legends

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature07821

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.