Superior Colliculus Neuronal Ensemble Activity Signals Optimal Rather Than Subjective Confidence

Abstract

Recent studies suggest that neurons in sensorimotor circuits involved in perceptual decision-making also play a role in decision confidence. In these studies, confidence is often considered to be an optimal readout of the probability that a decision is correct. However, the information leading to decision accuracy and the report of confidence often co-varied, leaving open the possibility that there are actually two dissociable signal types in the brain: signals that correlate with decision accuracy (optimal confidence) and signals that correlate with subjects behavioral reports of confidence (subjective confidence). We recorded neuronal activity from a sensorimotor decision area, the superior colliculus (SC) of monkeys, while they performed two different tasks. In our first task, decision accuracy and confidence co-varied, as in previous studies. In our second task, we implemented a novel motion discrimination task with stimuli that were matched for decision accuracy but produced different levels of confidence as reflected by behavioral reports. We used a multivariate decoder to predict monkeys choices from neuronal population activity. As in previous studies on perceptual decision-making mechanisms, we found that neuronal decoding performance increased as decision accuracy increased. However, when decision accuracy was matched, performance of the decoder was similar between high and low subjective confidence conditions. These results show that the SC likely signals optimal decision confidence similar to previously reported cortical mechanisms, but is unlikely to play a critical role in subjective confidence. The results also motivate future investigations to determine where in the brain signals related to subjective confidence reside.\n\nSignificance StatementConfidence is thought to reflect the rational or optimal belief concerning ones choice accuracy. Here, we introduce a novel version of the dot-motion discrimination task with stimulus conditions that produce similar accuracy but different subjective behavioral reports of confidence. We decoded decision performance of this task from neuronal signals in the superior colliculus (SC), a subcortical region involved in decision-making. We found that SC activity signaled a perceptual decision for visual stimuli, with the strength of this activity reflecting decision accuracy, but not the subjective level of confidence as reflected by behavioral reports. These results demonstrate an important role for the SC in perceptual decision-making and challenge current ideas about how to measure subjective confidence in monkeys and humans.