Pupil size predicts exploration through critical slowing in prefrontal dynamics

Area of Science:

• Neuroscience
• Cognitive Science
• Decision Making

Background:

• Intelligent decision-making involves balancing exploitation and exploration in uncertain environments.
• Pupil size is a potential correlate of neuromodulatory tone and arousal, linked to exploration.
• Previous research suggests pupil size may track factors influencing exploration (e.g., volatility, reward) rather than exploration itself.

Purpose of the Study:

• To investigate the direct relationship between pupil size and the initiation of exploration.
• To examine how pupil size predicts neural activity in the prefrontal cortex during exploration and exploitation.
• To test whether pupil size independently predicts exploration beyond reward history.

Main Methods:

• Simultaneous measurement of pupil size, behavioral exploration/exploitation, and prefrontal cortex neural population activity.
• Utilized a dynamic environment task with two male rhesus macaques.
• Controlled for luminance to isolate the effects of pupil size on exploration.

Main Results:

• Pupil size under constant luminance specifically predicted the onset of exploration, independent of reward history.
• Pupil size changes were correlated with disorganized neural activity patterns in the prefrontal cortex at both single neuron and population levels.
• Findings support a model where pupil-linked mechanisms facilitate exploration.

Conclusions:

• Pupil size serves as a specific predictor of exploration onset.
• Pupil-linked mechanisms may drive exploration by altering prefrontal cortex dynamics, potentially pushing them towards a critical tipping point.
• This research provides novel insights into the neural underpinnings of exploration and decision-making under uncertainty.