Schriver Brian J, Bagdasarov Svetlana, Wang Qi
Department of Biomedical Engineering, Columbia University , New York, New York.
J Neurophysiol. 2018 Oct 1;120(4):1655-1670. doi: 10.1152/jn.00290.2018. Epub 2018 Jul 11.
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.
非亮度介导的瞳孔大小变化已被广泛用于指示唤醒状态。最近的动物研究表明，行为状态相关的瞳孔动态与感觉处理之间存在相关性。然而，在执行感知任务的动物中，瞳孔相关的唤醒与行为之间的关系尚未完全阐明。在本研究中，我们训练头部固定的大鼠使用Go/No-Go辨别范式来辨别触须运动的方向，同时对它们的瞳孔进行成像。该辨别任务中的反应时间明显慢于之前报道的具有类似设置的检测任务，这表明辨别需要增加认知负荷。我们发现，在刺激呈现后的所有试验中，瞳孔都会扩张。有趣的是，在正确拒绝试验中，瞳孔扩张仅由认知处理引起，对于更难的刺激，扩张幅度更大。刺激呈现前的基线瞳孔大小与行为密切相关，因为感知灵敏度在中等瞳孔基线时达到峰值，而反应时间在大基线时最快。我们通过研究瞳孔基线在多大程度上能够预测即将发生的行为，进一步探索了这些关系，发现贝叶斯解码器在正确预测行为结果方面具有显著高于随机概率的可能性。此外，前一次试验的结果与当前试验的行为表现出强烈的相关性。在击中试验后，动物的反应更宽松、更快，而在正确拒绝试验后，感知灵敏度最高。综上所述，这些结果表明，行为大鼠的瞳孔动态、感知性能和反应时间之间存在紧密的相关性，所有这些都受到波动的唤醒状态的调节。新发现与值得注意之处 在本研究中，我们首次证明头部固定的大鼠能够辨别触须运动的不同方向。有趣的是，我们发现，在辨别更难的刺激时，瞳孔扩张得更多，这一现象在人类受试者中已有报道，但在动物中尚未报道。我们发现，刺激呈现前的基线瞳孔大小与行为密切相关，并且基于基线瞳孔大小的贝叶斯解码器在正确预测行为结果方面具有显著高于随机概率的可能性。
