Claron Julien, Royo Julie, Arcizet Fabrice, Deffieux Thomas, Tanter Mickael, Pouget Pierre
Physics for Medicine, ESPCI, INSERM, CNRS, PSL Research University, Paris, France.
Institut du Cerveau, INSERM 1127, CNRS 7225 Sorbonne Université, Paris, France.
PLoS Biol. 2022 May 26;20(5):e3001654. doi: 10.1371/journal.pbio.3001654. eCollection 2022 May.
In both human and nonhuman primates (NHP), the medial prefrontal region, defined as the supplementary eye field (SEF), can indirectly influence behavior selection through modulation of the primary selection process in the oculomotor structures. To perform this oculomotor control, SEF integrates multiple cognitive signals such as attention, memory, reward, and error. As changes in pupil responses can assess these cognitive efforts, a better understanding of the precise dynamics by which pupil diameter and medial prefrontal cortex activity interact requires thorough investigations before, during, and after changes in pupil diameter. We tested whether SEF activity is related to pupil dynamics during a mixed pro/antisaccade oculomotor task in 2 macaque monkeys. We used functional ultrasound (fUS) imaging to examine temporal changes in brain activity at the 0.1-s time scale and 0.1-mm spatial resolution concerning behavioral performance and pupil dynamics. By combining the pupil signals and real-time imaging of NHP during cognitive tasks, we were able to infer localized cerebral blood volume (CBV) responses within a restricted part of the dorsomedial prefrontal cortex, referred to as the SEF, an area in which antisaccade preparation activity is also recorded. Inversely, SEF neurovascular activity measured by fUS imaging was found to be a robust predictor of specific variations in pupil diameter over short and long-time scales. Furthermore, we directly manipulated pupil diameter and CBV in the SEF using reward modulations. These results bring a novel understanding of the physiological links between pupil and SEF, but it also raises questions about the role of anterior cingulate cortex (ACC), as CBV variations in the ACC seems to be negligible compared to CBV variations in the SEF.
在人类和非人类灵长类动物（NHP）中，内侧前额叶区域被定义为辅助眼区（SEF），它可以通过调节动眼结构中的初级选择过程来间接影响行为选择。为了执行这种动眼控制，SEF整合了多种认知信号，如注意力、记忆、奖励和错误信号。由于瞳孔反应的变化可以评估这些认知活动，因此在瞳孔直径变化之前、期间和之后进行全面研究，才能更好地理解瞳孔直径与内侧前额叶皮质活动相互作用的精确动态过程。我们测试了在2只猕猴进行混合的正/反扫视动眼任务期间，SEF活动是否与瞳孔动态相关。我们使用功能超声（fUS）成像来检查在行为表现和瞳孔动态方面，大脑活动在0.1秒时间尺度和0.1毫米空间分辨率下的时间变化。通过在认知任务期间结合瞳孔信号和NHP的实时成像，我们能够推断在背内侧前额叶皮质的一个受限部分内的局部脑血容量（CBV）反应，该部分被称为SEF，在这个区域也记录到了反扫视准备活动。相反，通过fUS成像测量的SEF神经血管活动被发现是短时间和长时间尺度上瞳孔直径特定变化的有力预测指标。此外，我们使用奖励调制直接操纵SEF中的瞳孔直径和CBV。这些结果为瞳孔与SEF之间的生理联系带来了新的认识，但同时也引发了关于前扣带回皮质（ACC）作用的问题，因为与SEF中的CBV变化相比，ACC中的CBV变化似乎可以忽略不计。
