Letter

Nature 459, 89-92 (7 May 2009) | doi:10.1038/nature07821; Received 29 October 2008; Accepted 23 January 2009; Published online 8 March 2009

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

Hendrikje Nienborg1 & Bruce G. Cumming1

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

Correspondence to: Hendrikje Nienborg1 Correspondence and requests for materials should be addressed to H.N. (Email: hnienb@gmail.com).

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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