Pupil-linked arousal modulates behavior in rats performing a whisker deflection direction discrimination task

• Published in: Journal of neurophysiology Vol. 120; no. 4; pp. 1655 - 1670
• Main Authors: Schriver, Brian J., Bagdasarov, Svetlana, Wang, Qi
• Format: Journal Article
• Language: English
• Published: United States American Physiological Society 01.10.2018
• Series: Higher Neural Functions and Behavior
• Subjects: Animals; Arousal; Discrimination, Psychological; Female; Movement; Muscle Relaxation; Pupil - physiology; Rats; Rats, Sprague-Dawley; Vibrissae - physiology; discrimination task; whisker system; signal detection theory; pupil dynamics; arousal
• DOI: 10.1152/jn.00290.2018
• ISSN: 0022-3077; 1522-1598

Non-luminance-mediated changes in pupil size have been widely used to index arousal state. Recent animal studies have demonstrated correlations between behavioral state-related pupil dynamics and sensory processing. However, the relationship between pupil-linked arousal and behavior in animals performing perceptual tasks has not been fully elucidated. In the present study, we trained head-fixed rats to discriminate between directions of whisker movements using a Go/No-Go discrimination paradigm while imaging their pupils. Reaction times in this discrimination task were significantly slower than in previously reported detection tasks with similar setup, suggesting that discrimination required an increased cognitive load. We found the pupils dilated for all trials following stimulus presentation. Interestingly, in correct rejection trials, where pupil dilations solely resulted from cognitive processing, dilations were larger for more difficult stimuli. Baseline pupil size before stimulus presentation strongly correlated with behavior, as perceptual sensitivity peaked at intermediate pupil baselines and reaction time was fastest at large baselines. We further explored these relationships by investigating to what extent pupil baseline was predictive of upcoming behavior and found that a Bayesian decoder had significantly greater-than-chance probability in correctly predicting behavioral outcomes. Moreover, the outcome of the previous trial showed a strong correlation with behavior on present trials. Animals were more liberal and faster in responding following hit trials, whereas perceptual sensitivity was greatest following correct rejection trials. Taken together, these results suggest a tight correlation between pupil dynamics, perceptual performance, and reaction time in behaving rats, all of which are modulated by fluctuating arousal state. NEW & NOTEWORTHY In this study, we for the first time demonstrated that head-fixed rats were able to discriminate different directions of whisker movement. Interestingly, we found that the pupil dilated more when discriminating more difficult stimuli, a phenomenon reported in human subjects but not in animals. Baseline pupil size before stimulus presentation was found to strongly correlate with behavior, and a Bayesian decoder had significantly greater-than-chance probability in correctly predicting behavioral outcomes based on the baseline pupil size.