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

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.

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Figure 1: Methods.
Figure 2: Psychophysical kernel and choice-related signal have different time courses.
Figure 3: Choice-dependent gain change.
Figure 4: Reward size affects behaviour and choice-related signal.

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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.

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Correspondence to Hendrikje Nienborg.

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This file contains Supplementary Methods and Results, a Supplementary Discussion, Supplementary References and Supplementary Figures 1-6 with Legends (PDF 208 kb)

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Nienborg, H., Cumming, B. Decision-related activity in sensory neurons reflects more than a neuron’s causal effect. Nature 459, 89–92 (2009). https://doi.org/10.1038/nature07821

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