Pupil size predicts the onset of exploration and changes in prefrontal dynamics

In uncertain environments, intelligent decision-makers exploit actions that have been rewarding in the past, but also explore actions that could be even better. Several neuromodulatory systems are implicated in exploration, based, in part, on work linking exploration to pupil size-a peripheral correlate of neuromodulatory tone and index of arousal. However, pupil size could instead track variables that make exploration more likely, like volatility or reward, without directly predicting either exploration or its neural bases. Here, we simultaneously measured pupil size, exploration, and neural population activity in the prefrontal cortex while two rhesus macaques explored and exploited in a dynamic environment. We found that pupil size under constant luminance specifically predicted the onset of exploration, the first exploratory trial in a sequence, beyond what could be explained by reward history. Pupil size also predicted disorganized patterns of prefrontal neural activity at both the single neuron and population levels, even within periods of exploitation. Ultimately, our results support a model in which pupil-linked mechanisms promote the onset of exploration via driving the prefrontal cortex through a critical tipping point where prefrontal control dynamics become disorganized and exploratory decisions are possible. Significance StatementHumans and other animals learn about the world through exploration: through making decisions that offer the opportunity to learn and discover, even when these decisions are not the best option in the moment. Neuroscience research has historically focused on understanding good choices, delivering many key insights into the neural mechanisms involved in these calculations. However, much less is known about how the brain generates exploratory decisions. This study identifies certain "early warning signs" of exploratory decisions in the brain and body, including certain signals in size of the pupil and the speed of neural activity in the prefrontal cortex. These early warning signs suggest that exploration may be the result of a critical tipping point in prefrontal brain states.