Division of Endocrinology, Diabetes, and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA; F.M. Kirby Neurobiology Center, Boston Children's Hospital, Harvard Medical School, Boston, MA 02115, USA.
Division of Endocrinology, Diabetes, and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA; School of Life Science, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne 1015, Switzerland.
Curr Biol. 2020 Oct 19;30(20):3923-3934.e9. doi: 10.1016/j.cub.2020.07.065. Epub 2020 Aug 13.
The brain can flexibly filter out sensory information in a manner that depends on behavioral state. In the visual thalamus and cortex, arousal and locomotion are associated with changes in the magnitude of responses to visual stimuli. Here, we asked whether such modulation of visual responses might already occur at an earlier stage in this visual pathway. We measured neural activity of retinal axons using wide-field and two-photon calcium imaging in awake mouse thalamus across arousal states associated with different pupil sizes. Surprisingly, visual responses to drifting gratings in retinal axonal boutons were robustly modulated by arousal level in a manner that varied across stimulus dimensions and across functionally distinct subsets of boutons. At low and intermediate spatial frequencies, the majority of boutons were suppressed by arousal. In contrast, at high spatial frequencies, boutons tuned to regions of visual space ahead of the mouse showed enhancement of responses. Arousal-related modulation also varied with a bouton's preference for luminance changes and direction or axis of motion, with greater response suppression in boutons tuned to luminance decrements versus increments, and in boutons preferring motion along directions or axes of optic flow. Together, our results suggest that differential modulation of distinct visual information channels by arousal state occurs at very early stages of visual processing, before the information is transmitted to neurons in visual thalamus. Such early filtering may provide an efficient means of optimizing central visual processing and perception across behavioral contexts.
大脑可以灵活地以依赖于行为状态的方式过滤感觉信息。在视觉丘脑和皮质中,觉醒和运动与视觉刺激反应幅度的变化有关。在这里,我们询问这种对视觉反应的调制是否可能已经在这个视觉通路的早期阶段发生。我们使用广角和双光子钙成像技术,在觉醒的小鼠丘脑内测量了视网膜轴突的神经活动,跨越了与不同瞳孔大小相关的觉醒状态。令人惊讶的是,视网膜轴突末梢的漂移光栅的视觉反应被觉醒水平以一种跨刺激维度和功能上不同的末梢亚群变化的方式强烈地调制。在低和中频空间频率下,大多数末梢被觉醒抑制。相比之下,在高空间频率下,对鼠标前方视觉区域调谐的末梢表现出反应增强。与觉醒相关的调制也随着末梢对亮度变化和运动方向或轴的偏好而变化,对亮度降低调谐的末梢的反应抑制大于对亮度增加调谐的末梢,并且对沿光流方向或轴运动的末梢偏好更大。总的来说,我们的结果表明,不同的视觉信息通道的调制在视觉处理的早期阶段,在信息传递到视觉丘脑的神经元之前,就由觉醒状态决定。这种早期过滤可能为优化不同行为情境下的中央视觉处理和感知提供了一种有效的手段。