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 identical 1– 9. The origin of this correlation is unknown. Current theory proposes a causal effect of noise in sensory neurons on perceptual decisions 10– 12, but it could result from different brain-states associated with the perceptual choice 13 (top-down). These two schemes have very different implications for the role played by sensory neurons in forming decisions 14. Here, we used white-noise analysis 15 to measure tuning-functions of V2 neurons associated with choice and simultaneously measure how the variation in the stimulus affects subjects’ (two macaques) perceptual decisions 16– 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 timecourse of the trial, these measures change in different directions—at odds with causal models. An analysis of effect of reward size supports the same conclusion. Finally, choice was 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 attention 19. 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.