Pupil-linked arousal modulates precision of representation in cortex

Cortical responses fluctuate over time, even when the stimulus is held constant. Accordingly, the amount of information contained in activity varies too, with important consequences for behavior. What processes might underlie these fluctuations in the cortical representation of a stimulus? We hypothesized that one factor underlying response variability could be spontaneous changes in arousal state. We tested the hypothesis using a combination of fMRI, probabilistic decoding methods and pupillometry. Human observers were presented with gratings of random orientation (0-179 degrees). Shortly after stimulus presentation, they reported the orientation of the viewed grating. Pupil size was recorded to index the observer’s arousal state. To quantify the degree of imprecision in the orientation representation, we decoded trial-by-trial probability distributions from activity in visual cortex (V1-V3), taking distribution width as a measure of orientation uncertainty. Replicating previous studies, the width of the decoded distribution varied over trials and predicted the observer’s behavioral performance. To assess whether these changes in the fidelity of the cortical representation could be driven by arousal state, we correlated decoded uncertainty with pupil size. Interestingly, we observed a reliable inverse relationship between pupil size and the degree of uncertainty in cortex. Thus, when pupil size was larger – indicating higher levels of arousal – the cortical representation of the presented stimulus was more precise. This suggests that spontaneous fluctuations in arousal impact the fidelity of the cortical stimulus representation, and provides further insight into the mechanisms that create perceptual uncertainty.