Dissociation of Choice Formation and Choice-Correlated Activity in Macaque Visual Cortex

Responses of individual task-relevant sensory neurons can predict monkeys' trial-by-trial choices in perceptual decision-making tasks. Choice-correlated activity has been interpreted as evidence that the responses of these neurons are causally linked to perceptual judgments. To further test this hypothesis, we studied responses of orientation-selective neurons in V1 and V2 while two macaque monkeys performed a fine orientation discrimination task. Although both animals exhibited a high level of neuronal and behavioral sensitivity, only one exhibited choice-correlated activity. Surprisingly, this correlation was negative: when a neuron fired more vigorously, the animal was less likely to choose the orientation preferred by that neuron. Moreover, choice-correlated activity emerged late in the trial, earlier in V2 than in V1, and was correlated with anticipatory signals. Together, these results suggest that choice-correlated activity in task-relevant sensory neurons can reflect postdecision modulatory signals.

SIGNIFICANCE STATEMENT When observers perform a difficult sensory discrimination, repeated presentations of the same stimulus can elicit different perceptual judgments. This behavioral variability often correlates with variability in the activity of sensory neurons driven by the stimulus. Traditionally, this correlation has been interpreted as suggesting a causal link between the activity of sensory neurons and perceptual judgments. More recently, it has been argued that the correlation instead may originate in recurrent input from other brain areas involved in the interpretation of sensory signals. Here, we call both hypotheses into question. We show that choice-related activity in sensory neurons can be highly variable across observers and can reflect modulatory processes that are dissociated from perceptual decision-making.

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