Abstract

Trial-by-trial correlations between neural responses and choices (choice probabilities) are often interpreted to reflect a causal contribution of neurons to task performance. However, choice probabilities may arise from top-down, rather than bottom-up, signals. We isolated distinct sensory and decision contributions to single-unit activity recorded from the dorsal medial superior temporal (MSTd) and ventral intraparietal (VIP) areas of monkeys during perception of self-motion. Superficially, neurons in both areas show similar tuning curves during task performance. However, tuning in MSTd neurons primarily reflects sensory inputs, whereas choice-related signals dominate tuning in VIP neurons. Importantly, the choice-related activity of VIP neurons is not predictable from their stimulus tuning, and these factors are often confounded in choice probability measurements. This finding was confirmed in a subset of neurons for which stimulus tuning was measured during passive fixation. Our findings reveal decoupled stimulus and choice signals in the VIP area, and challenge our understanding of choice signals in the brain.

Highlights

  • Trial-by-trial correlations between neural responses and choices are often interpreted to reflect a causal contribution of neurons to task performance

  • This result has been corroborated by widespread findings of significant choice probabilities (CPs; a metric that quantifies the relationship between neuronal activity and perceptual decisions across repeated presentation of a stimulus) in many cortical areas[1, 4,5,6,7,8,9,10] and recently, even subcortically[11]

  • Our results demonstrate a predominance of choice signals in ventral intraparietal (VIP), with a large unique contribution that is uncorrelated with the relevant sensory signals

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Summary

Introduction

Trial-by-trial correlations between neural responses and choices (choice probabilities) are often interpreted to reflect a causal contribution of neurons to task performance. For a neuron that prefers rightward motion stimuli, an above average response to a given stimulus should bias the animal’s choice toward rightward in such a feedforward scheme This produces values of CP > 0.5, by the usual convention in which CPs are computed, reflecting that choice-related modulations are in the same direction as the cell’s tuning. We show that CPs are a poor means to answer this question This is because of a potential logical flaw: if top-down (choice related) signals are present in neuronal activity, these choice signals influence the tuning curve from which a neuron’s stimulus preference is determined (and used to compute CP). It is imperative to separate and quantify the concurrent influences of sensory and decision signals

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