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

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Abstract
The ability of sensory neurons to predict an animal's upcoming decision has generated enormous interest over the past decade, and the impression has grown that the activity of these neurons in some way causes the appropriate decision to be made. Now in a study involving monkeys making choices in a video-based binocular-disparity discrimination task, Hendrikje Nienborg and Bruce Cumming show that this model is too simplistic. Their data reveal an opposite direction of causality: once a decision is made, the decision itself changes the responses of the sensory neurons. Deciding what one sees actively changes what is seen. The ability of sensory neurons to predict an animal's upcoming decision has generated enormous interest over the last 10 years, with the proposal being that the activity of these neurons causes the appropriate decision to be made. Measuring neuronal tuning curves and perceptual decisions in a visual discrimination task in macaque monkeys, decision making was found to change the responses in sensory neurons in a 'top-down' manner, consistent with the effects of attention, thus indicating that this model is too simplistic. 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.