Letter | Published:

Distinct relationships of parietal and prefrontal cortices to evidence accumulation

Nature volume 520, pages 220223 (09 April 2015) | Download Citation

Abstract

Gradual accumulation of evidence is thought to be fundamental for decision-making, and its neural correlates have been found in several brain regions1,2,3,4,5,6,7,8. Here we develop a generalizable method to measure tuning curves that specify the relationship between neural responses and mentally accumulated evidence, and apply it to distinguish the encoding of decision variables in posterior parietal cortex and prefrontal cortex (frontal orienting fields, FOF). We recorded the firing rates of neurons in posterior parietal cortex and FOF from rats performing a perceptual decision-making task. Classical analyses uncovered correlates of accumulating evidence, similar to previous observations in primates and also similar across the two regions. However, tuning curve assays revealed that while the posterior parietal cortex encodes a graded value of the accumulating evidence, the FOF has a more categorical encoding that indicates, throughout the trial, the decision provisionally favoured by the evidence accumulated so far. Contrary to current views3,5,7,8,9, this suggests that premotor activity in the frontal cortex does not have a role in the accumulation process, but instead has a more categorical function, such as transforming accumulated evidence into a discrete choice. To probe causally the role of FOF activity, we optogenetically silenced it during different time points of the trial. Consistent with a role in committing to a categorical choice at the end of the evidence accumulation process, but not consistent with a role during the accumulation itself, a behavioural effect was observed only when FOF silencing occurred at the end of the perceptual stimulus. Our results place important constraints on the circuit logic of brain regions involved in decision-making.

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References

  1. 1.

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

  2. 2.

    & Caudate encodes multiple computations for perceptual decisions. J. Neurosci. 30, 15747–15759 (2010)

  3. 3.

    & Neural correlates of perceptual decision making before, during, and after decision commitment in monkey frontal eye field. Cereb. Cortex 22, 1052–1067 (2012)

  4. 4.

    & Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. J. Neurophysiol. 86, 1916–1936 (2001)

  5. 5.

    & Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque. Nature Neurosci. 2, 176–185 (1999)

  6. 6.

    , , , & Dual diffusion model for single-cell recording data from the superior colliculus in a brightness-discrimination task. J. Neurophysiol. 97, 1756–1774 (2007)

  7. 7.

    et al. Neurally constrained modeling of perceptual decision making. Psychol. Rev. 117, 1113–1143 (2010)

  8. 8.

    , , & Context-dependent computation by recurrent dynamics in prefrontal cortex. Nature 503, 78–84 (2013)

  9. 9.

    & Neural mechanisms of speed-accuracy tradeoff. Neuron 76, 616–628 (2012)

  10. 10.

    , & Rats and humans can optimally accumulate evidence for decision-making. Science 340, 95–98 (2013)

  11. 11.

    & Response of neurons in the lateral intraparietal area during a combined visual discrimination reaction time task. J. Neurosci. 22, 9475–9489 (2002)

  12. 12.

    , , , & Navigating from hippocampus to parietal cortex. Proc. Natl Acad. Sci. USA 105, 14755–14762 (2008)

  13. 13.

    , & A cortical substrate for memory-guided orienting in the rat. Neuron 72, 330–343 (2011)

  14. 14.

    et al. Cortical representation of motion during unrestrained spatial navigation in the rat. Cereb. Cortex 4, 27–39 (1994)

  15. 15.

    , , , & Functional split between parietal and entorhinal cortices in the rat. Neuron 73, 789–802 (2012)

  16. 16.

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

  17. 17.

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

  18. 18.

    & Intention, action planning, and decision making in parietal-frontal circuits. Neuron 63, 568–583 (2009)

  19. 19.

    , & A category-free neural population supports evolving demands during decision-making. Nature Neurosci. 17, 1784–1792 (2014)

  20. 20.

    et al. Flow of cortical activity underlying a tactile decision in mice. Neuron 81, 179–194 (2014)

  21. 21.

    , , , & Chemically etched fiber tips for near-field optical microscopy: a process for smoother tips. Appl. Opt. 37, 7289–7292 (1998)

  22. 22.

    et al. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141, 154–165 (2010)

  23. 23.

    The prefrontal cortex of the rat. I. Cortical projection of the mediodorsal nucleus. II. Efferent connections. Brain Res. 12, 321–343 (1969)

  24. 24.

    et al. The organization of the rat motor cortex: a microstimulation mapping study. Brain Res. 11, 77–96 (1986)

  25. 25.

    The corticocortical projections of the physiologically defined eye field in the rat medial frontal cortex. Brain Res. Bull. 47, 377–385 (1998)

  26. 26.

    , , & Prefrontal contributions to visual selective attention. Annu. Rev. Neurosci. 36, 451–466 (2013)

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Acknowledgements

We thank K. Deisseroth for support with optogenetics. We thank A. Akrami, T. Buschman, J. Gold, B. Pesaran, B. Scott, D. Tank and M. Yartsev for comments on the manuscript. We thank A. Begelfer, K. Osorio and J. Teran for animal and laboratory support. T.D.H. was supported by National Institutes of Health (NIH) Award Number F32MH098572. C.A.D. was supported by a Howard Hughes Medical Institute predoctoral fellowship. C.D.K. was supported in part by the NIH Award Number T32MH065214.

Author information

Author notes

    • Timothy D. Hanks
    •  & Charles D. Kopec

    These authors contributed equally to this work.

Affiliations

  1. Princeton Neuroscience Institute, Princeton University, Princeton, New Jersey 08544, USA

    • Timothy D. Hanks
    • , Charles D. Kopec
    • , Bingni W. Brunton
    • , Chunyu A. Duan
    • , Jeffrey C. Erlich
    •  & Carlos D. Brody
  2. Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544, USA

    • Timothy D. Hanks
    • , Charles D. Kopec
    • , Bingni W. Brunton
    • , Chunyu A. Duan
    • , Jeffrey C. Erlich
    •  & Carlos D. Brody
  3. Departments of Biology and Applied Mathematics, University of Washington, Seattle, Washington 98105, USA

    • Bingni W. Brunton
  4. NYU-ECNU Institute of Brain and Cognitive Science, NYU-Shanghai, Shanghai 200122, China

    • Jeffrey C. Erlich
  5. Howard Hughes Medical Institute, Princeton University, Princeton, New Jersey 08544, USA

    • Carlos D. Brody

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Contributions

T.D.H., B.W.B., C.A.D. and J.C.E. collected electrophysiological data. T.D.H. analysed electrophysiological data. J.C.E. played an advisory role on electrophysiological experiments. C.D.K. carried out the optogenetic experiments, with assistance from B.W.B. C.D.K. analysed the optogenetics data, with input and assistance from T.D.H. and J.C.E. T.D.H., C.D.K. and C.D.B. wrote the paper. C.D.B. was involved in all aspects of experimental design and data analysis.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Carlos D. Brody.

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https://doi.org/10.1038/nature14066

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